Origin and Evolution of Insect Wings and Their Relation to Metamorphosis, as Documented by the Fossil Record

JARMILA KUKALOVA-PECK Department of Geology, Carleton University, Ottawa, Ontario KlS 5B6 Canada

TABLE OF CONTENTS

Abstract 53 Introduction ...... 55 I. Origin and evolution of wing structures . . 57 Origin of wings and flight.. , , , ...... , ...... 57 Principle of recapitulation ...... 57 The paranotal theory ...... 59 Fossil and comparative-morphological evidence 60 Summary of evidence against paranotal theory ...... , . . . . . , 62 Pretracheation theory of Comstock-Needham ...... , . . . , , , 64 Spiracular flap theory . . . , , , ...... , , . 66 Stylus theory ...... , . . , 67 Fin theory ...... 69 Gill-cover theory ...... 70 Synthesis of ideas on wing evolution ...... 71 Introduction to wing venation ...... 73 Origin of wing corrugation ...... , 76 Flight efficiency ...... 78 11. Origin and development of the alar circulatory system ...... 79 Circulatory system in modern and p tive wings of juveniles 79 Evolutionary changes in blood flow . , . . , ...... , . , , . , , 80

111. Origin of wing articulation ...... , 81 Interpretation of pteralia in primitive Palaeodictyoptera . . . . 81

IV. Wings and metamorphosis ...... , , 84 Primitive position of wings in nymphs ...... 84 Primitive position of wings in adults ...... 85 Onset of metamorphosis ...... 87 V. Principles of irreversibility and irrevocability of evolution . . . . . 90 VI. Wings and taxonomy ...... 91 Differential diagnosis of Paleoptera and Neoptera . . . . , . 91 Monophyly and parallel development in Pterygota ...... 92

ABSTRACT In contemporary entomology the morphological characters of in- sects are not always treated according to their phylogenetic rank. Fossil evidence often gives clues for different interpretations. All primitive Paleozoic pterygote nymphs are now known to have had articulated, freely movable wings reinforced by tubular veins. This suggests that the wings of early Pterygota were engaged in flapping movements, that the immobilized, fixed, veinless wing pads of Recent nymphs have resulted from a later adaptation affecting only juveniles, and that theparanotal theory of wing origin is not valid. The wings of Paleozoic nymphs

J. MORPH. (1978) 156: 53-126. 53 54 JARMILA KUKALOVA-PECK

were curved backwards in Paleoptera and were flexed backwards at will in Neop- tera, in both to reduce resistance during forward movement. Therefore, the fixed oblique-backwards position of wing pads in all modern nymphs is secondary and is not homologous in Paleoptera and Neoptera. Primitive Paleozoic nymphs had articulated and movable prothoracic wings which became in some modern insects transformed into prothoracic lobes and shields. The nine pairs of abdominal gill- plates of Paleozoic mayfly nymphs have a venation pattern, position, and deuelop- ment comparable to that in thoracic wings, to which they are serially homologous. Vestigial equivalents of wings and legs were present in the abdomen of all primi- tive Paleoptera and primitive Neoptera. The ontogenetic development of Paleozoic nymphs was confluent, with many nymphal and subimaginal instars, and the metamorphic instar was missing. The metamorphic instar originated by the merging together of several instars of old nymphs; it occurred in most orders only after the Paleozoic, separately and in parallel in all modern major lineages (at least twice in Paleoptera, in Ephemeroptera and Odonata; separately in hemipteroid, blattoid, orthopteroid, and plecopteroid lineages of exopterygote Neoptera; and once only in Endopterygota). Endopterygota evolved from ametabolous, not from hemimetabolous, exopterygote Neoptera. The full primitive wing venation consists of six symmetrical pairs of veins; in each pair, the first branch is always convex and the second always concave; there- fore costa, subcosta, radius, media, cubitus, and anal are all primitively com- posed of two separate branches. Each pair arises from asingle veinal base formed from a sclerotized blood sinus. In the most primitive wings the circulatory system was as follows: the costa did not encircle the wing, the axillary cord was missing, and the blood pulsed in and out of each of the six primary, convex-concave vein pair systems through the six basal blood sinuses. This type of circulation is found as an archaic feature in modern mayflies. Wing corrugation first appeared in pre- flight wings, and hence is considered primitive for early (paleopterous) Ptery- gota. Somewhat leveled corrugation of the central wing veins is primitive for Neoptera. Leveled corrugation in some modern Ephemeroptera, as well as accen- tuated corrugation in higher Neoptera, are both derived characters. The wing tracheation of Recent Ephemeroptera is not fully homologous to that of other in- sects and represents a more primitive, segmental stage of tracheal system. Morphology of an ancient articular region in Palaeodictyoptera shows that the primitive pterygote wing hinge in its simplest form was straight and composed of two separate but adjoining morphological units: the tergal, formed by the tegula and axillaries; and the alar, formed by six sclerotized blood sinuses, the basi- venales. The tergal sclerites were derived from the tergum as follows: the lateral part of the tergum became incised into five lobes; the prealare, suralare, median lobe, postmedian lobe and posterior notal wing process. From the tips of these lobes, five slanted tergal sclerites separated along the deep paranotal sulcus: the tegula, first axillary, second axillary, median sclerite, and third axillary. Primi- tively, all pteralia were arranged in two parallel series on both sides of the hinge. In Paleoptera, the series stayed more or less straight; in Neoptera, the series became V-shaped.Pteralia in Paleoptera and Neoptera have been homologized on the basis of the fossil record. A differential diagnosis between Paleoptera and Neoptera is given. Fossil evi- dence indicates that the major steps in evolution, which led to the origin first of Pterygota, then of Neoptera and Endopterygota, were triggered by the origin and the diversification offlight apparatus. It is believed here that all above mentioned major events in pterygote evolution occurred first in the immature stages. INSECT WINGS. METAMORPHOSIS, AND THE FOSSIL RECORD 55

INTRODUCTION tematic ladder (the highly specialized “bi- Recently, it was written: “It is obvious, of focal” eyes and fore legs of a mayfly male do course, that the natural phylogeny of insects not effect or alter the fact that Ephemerop- is to be found in the fossil record. However, tera are the most primitive pterygote order, while the fossil history of the various insect etc.). Strictly speaking, the character state orders is becoming fairly well known in a gross present in the ancestor is primitive while any sense . . . , to date, paleontology has not given change from this condition is derived. How- us any of the phylogenetic proof that we ever, in practice, deciding which character in require. We cannot resolve our differences by a given group of living organisms is primitive reference to the fossil record” (Scudder, ’73). and which one derived is often very difficult. These words of regret over the seemingly For instance, the extant representatives of an unsatisfactory state of knowledge of the fossil ancestral lineage might themselves have record showed that many entomologists view acquired newly derived characters, long after the benefits from paleoentomology to be main- it gave rise to the descendant lineage. These ly if not only in the delivery of missing links, might mistakenly be considered as primitive i.e., early representatives of evolutionary and the understanding of the respective de- lineages and unknown ancestors. Believing in scendant group (at any systematic level) a broad phylogenetic approach to entomologi- might be seriously impared. It should be there- cal problems, I searched for areas where fossil fore always kept in mind that, no matter how evidence is now available and where the fossil many primitive characters are present in a re- record can shed light upon the many sub- spective organism, there is no basis for the disciplines of entomology. It is necessary at anticipation that all should be primitive and the start to discuss some background opera- none derived. tional philosophy concerning insect evolution The correct categorization of characters is and morphology, because these viewpoints are often complicated by two related evolutionary closely interwoven with the development of phenomena: convergence and parallel evolu- the theses of this paper. tion. Parallelism includes similarities in two or more genetic lines which have been mainly The correct application of the phylogenetic channeled by a common ancestry, while con- approach to the natural system of classifica- vergent similarities have been caused prin- tion (Hennig, ’66) requires that the taxa cipally by environmental selective pressures should follow, step by step and in correct in less related groups. Of these two, con- sequence, the actual events of diversification vergence is better understood while parallel which took place in evolutionary history. evolution, though extremely widespread in Thus, in general, fossil insects occuring in the insects, has been given relatively little atten- Paleozoic contribute data on the highest taxa, tion. From parallel evolution stems, for in- such as supraordinal and ordinal, and their stance, the well known phenomenon that an diagnostic characteristics; Mesozoic fossils insect appears to be allied with certain rela- provide information on family and superfami- tives when one character is used, but with ly levels; Tertiary insects help to solve prob- others when a different character is consid- lems mostly at the generic level; and Quater- ered. Again, this phenomenon occurs at all nary fossil and subfossil insects are useful in systematic levels. Inevitably, parallelism the study of Recent species, including specia- causes more errors in morphological in- tion generated by climatic change and change terpretations than any other evolutionary fac- in geographic distribution. tor. But, the fossil record, by registering the The recognition of the proper categories of characters before or in the process of change, resemblance between morphological charac- has the potential to identify cases of paral- ters in relation to their phylogenetic sequence lelism and convergence, as well as the respec- is generally viewed as a major problem of tive categories of characters. modern systematics. In order to “categorize” Many examples are here given of presum- the characters it is necessary to recognize ably correct observations made by Recent them as “primitive” or as “derived,” at all re- morphologists. However, it is not the goal of spective subsequent systematic levels. Thus, this paper to base any conclusions entirely on an insect that is primitive within its ordinal the results of modern morphology. Informa- level might be highly derived within its speci- tion from comparative morphological studies fic level, or vice versa, throughout the sys- may be biased by anticipation, the incidence 56 JARMILA KUKALOVA-PECK of which is much more probable in the higher upward over their back). The first flying in- taxonomic levels, which are the concern of sects belonged to the Paleoptera which had a this paper, than in lower categories. The high- paleopterous alar articulation and a deep, reg- er taxa in the Pterygota reflect phylogenetic ular wing corrugation; in the Paleozoic they events which mostly took place some 300 to included the following orders: Palaeodictyop- 400 million years ago and an impressive adap- tera, Megasecoptera, Protodonata, Diaphan- tation of the basic characters changed many opterodea, Ephemeroptera and Odonata; only of them almost beyond recognition. Therefore, the last two are extant. Neoptera presumably the interpretations of Recent morphologists became derived from early Paleoptera by are here confronted with data present in the adapting one sclerite (the third axillary) fossil record, as is currently done with verte- which acquired a pivoting position and brates and many invertebrate groups other enabled the wings to be flexed backwards at than insects. will. This type of articulation is called neop- From the above-mentioned considerations it terous. The central alar veins (M, Rs) of Neop- should be clear that: (1) living forms provide tera are more or less flat and therefore the only indirect evidence for establishing the wing corrugation is not as regular as in natural system and for interpreting morpholo- Paleoptera. Fossil wings can be classified gy, (2) although it is tempting to arrange ex- according to this last feature even if frag- tant characters in a series of primitive and mented. Paleozoic Neoptera contained the advanced stages, series of this sort may con- orders: Protorthoptera (a large composite tain numerous errors, (3) comparative studies order including hemipteroid, blattoid, orthop- of the morphological features of living insects, teroid and plecopteroid types of primitive in- while they can provide a great amount of sects), Blattodea, Protelytroptera, Orthop- information, have always to be considered and tera, Caloneurodea, Plecoptera, Miomoptera, treated as indirect evidence for both tax- Hemiptera, Psocoptera, Neuroptera, Megalop- onomic and evolutionary morphological pur- tera, Glosselytrodea, Coleoptera, Mecoptera, poses, (4) living organisms are almost always and Trichoptera. Endopterygota supposedly mosaics of primitive and derived characters evolved from early exopterygote Neoptera. which resulted from adaptation to their par- Wings. Pro-wings, or preflight wings, are ticular ecology. Intricate adaptive processes the incipient but functional “wings” of early frequently obliterate the origin of these fea- flightless pterygotes which were present on tures, but the fossil record can present an im- all thoracic and abdominal segments; wing- mediate testimony to a particular phylogenet- lets are small (thoracic and abdominal) wings; ic state. prothoracic winglets were primitively func- In the present paper, I seek to show the com- tional, but were later immobilized, and plementary nature of modern comparative in- became transformed homologues of ptero- sect morphology and paleoentomology, in an thoracic and abdominal wings; gill-plates or attempt to harmonize the observations in both gill-covers are abdominal wings of some disciplines, and to draw some possible con- aquatic nymphs; veins are tubular, cuticular- clusions. ized and sclerotized thickenings which in the To help the reader understand the thesis to Paleozoic occured in the wings of both nymphs be developed, some phylogenetic concepts are and adults, but in the Recent are present only mentioned, which will be discussed and docu- in the adults; corrugation or fluting is the fan- mented later, and several terms are defined like folding of t,he wing so that the convex for clarity. veins ( + 1 form ribs rising above, and concave Phylogeny. Pterygota are considered to be veins (-) form grooves receding under, the descendent from the ancient Apterygota, wing plane; a given vein is always primitively ancestral to both Archaeognatha (including either convex or concave but it can become fossil Monura) and Thysanura. The alar artic- secondarily neutral (flat) by losing its cor- ulation in early flightless Pterygota, as rugation; mechanization of wing venation is a believed here, did not allow flexing of the inci- shifting of the costa, subcosta, and radius an- pient wings back over the body at rest. This teriorly and parallelly to support the anterior type of articulation is known as paleopterous margin as is essential in flying wings. (flexing of the wings should not be confused Metamorphosis. Most physiologists agree with the ability of some Recent Odonata and that metamorphosis is only that part of post- Ephemeroptera to fold their wings simply embryonic development which takes place in INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD 57 the absence of a morphogenetically active con- these questions and shows that some of the centration of juvenile hormone, i.e., the last previous hypotheses can be eliminated. larval instar of exopterygote Neoptera and both the last two larval instars (prepupa and Principle of recapitulation pupa) of Endopterygota. Ametabolous de- The correct interpretation of the principle velopment is a confluent ontogenetic develop- of recapitulation (partial recapitulation of ment in which moulting does not cease with phylogeny in ontogeny, following De Beer, ’58; the acquisition of sexual maturity and the Novak, ’66; and many others) is particularly metamorphic instar is missing; it occurs in important for a theory of the origin and early modern Apterygota and was probably present evolution of the wing. Formerly the more in all primitive (mostly Paleozoic) Pterygota; mature nymphs of hemimetabolous insects incremental (confluent, sequential) ontoge- were used for this purpose, but a comparison netic series of developmental stages are docu- of these nymphs with primitive Paleozoic mented for the Paleozoic orders, in which the nymphs has revealed that they have become increase in size between the first instar and too specialized, through adaptation to their the adult was completely confluent with nu- particular needs, to reflect their phylogeny merous subimaginal instars, so that the meta- (see section IV, Primitive position of wings). morphic instar was not “needed.” The multi- The recapitulation model of alar origin which ple origin of metamorphosis is the most proba- was based upon the morphology of older ble explanation for the fact that some living nymphs has led to confusion. For instance, the metabolous insect orders are documented to nymphal wing pads of Recent Ephemeroptera, have ametabolous Paleozoic ancestors with which are fused with the tergum and are fixed confluent ontogenetic development. “Nymph” in a lateroposterior position (fig. 29), were is used as a convenient morphological term for considered to be in the primitive position. the juveniles of Paleoptera and Neoptera- Therefore Lemche (’40, ’42; and followers) Exopterygota without implying a hypothesis concluded that Ephemeroptera are closely re- on metamorphosis. lated to Neoptera, that the Paleoptera are not I. Origin and evolution of wing structures monophyletic, that the Odonata are not monophyletic with other Pterygota and, as Origin of wings and flight another variant, that Ephemeroptera are in- Few events in the Animal Kingdom have termediate between Paleoptera and Neoptera. been the subject of as many hypotheses as the This is a misreading of secondarily derived origin of insect wings (for summaries, see features for a recapitulation of phylogenetic Alexander and Brown, ’63; Sharov, ’66; Wig- characters, and is contrary to the fossil evi- glesworth, ’76; Wootton, ’76). The aim of this dence that is now available (fig. 30). section is not to propose an additional hypoth- A more suitable recapitulation model, esis, attractive as this may be, but to review which is in agreement with the fossil evidence the fossil evidence that substantially limits of Paleozoic nymphs, was found in the the variety of plausible explanations of the ontogenetic development of younger nymphs origin of insect wings. of some Recent Paleoptera and Neoptera (in The fundamental questions are the follow- Odonata and Ephemeroptera by Bocharova- ing: 1. Are the wings “new” (pterygote) struc- Messner, ’59, ’65; in Hemiptera, Orthoptera tures or are they adapted “old’ (arthropod) and Blattodea by Tower, ’03). In the specimens structures? 2. If they are new structures, examined, the wings primitively started as what was their origin and primary function? epidermal thickenings, then evaginated as 3. If they are old structures, with what are (or wing-sacks or folds, and migrated during sev- were) they homologous in other arthropods? 4. eral moults towards the tergum, with which Are there abdominal appendages that are they eventually fused; at that point they came serially homologous with the thoracic wings? to acquire their appearance as older nymphs 5. What were the agents that promoted the (fig. 36, I-VIII). It was found that the wings preadaptation of the thoracic pro-wings for started as separate structures, independent flight, with respect to size, mechanized vena- from the tergum in younger nymphs, but tion, membranization, articulation, and mus- became fused with the tergum and immo- culature, before they were yet capable of fly- bilized in older nymphs; consequently they ing? Analysis of the fossil evidence now at cannot be paranota. hand provides a clearer insight into some of The sequence of stages in the development 58 JARMILA KUKALOVA-PECK of the wing of living Libellulidae and Aesh- made by Tower (’03).He found that the epider- nidae is, according to Bocharova-Messner mal alar thickening (wing disc) invariably ap- (’59),as follows: In the first nymphal instar, pears just above the spiracle in all pterygotes. the wing starts as an epidermal thickening In Anasa tristis (Hemiptera), the wing-discs whose location is marked externally only by arise in the embryos and are evaginated at the the presence of two prominent setae (fig. 36, time of the first moult. In Periplaneta (Blat- I). The thickening is located just above the todea), the epidermal wing-disc migrates dor- spiracle, lateral to, and well apart from the sally and posteriorly, and when it evaginates, tergum. In the second instar, a wing thicken- it imitates the postero-lateral paranotal lobe ing with two setae becomes slightly outlined. without being a homologous structure. In Mi- It increases in size and, with each successive crocentrum latifolium (Orthoptera) the wing instar, moves closer to the tergum. Sometime disc evaginates in the embryo beneath the during its upward migration, it evaginates to cuticle, but does not become external until form the actual wing bud. In about the sixth after the first nymphal moult. instar in Libellulidae and the fifth instar in Bocharova-Messner (’68) studied the on- Aeshnidae the wing bud finally reaches the togenetic development of the flight apparatus tergum and adjoins it laterally. Within the (the skeleton, the musculature, and the wing- next instars it enlarges and, at last, changes buds) in Blatta, Blattella, Gryllus, Oecanthus, into a flattened wing pad. The wing pad mi- Acheta, Perla, and Locusta. She confirmed grates upward on the segment and its apex Tower’s observations and found that the data eventually becomes directed backwards (fig. on wing development accumulated by her in 36, VIII). Only in this stage does the nymphal juvenile Paleoptera (’59,’65) are also valid for wing pad start to resemble the “paranotum” the Neoptera. She concluded that the de- and gain the postero-laterally oriented “neop- veloping wings in the nymphs became sec- terous” appearance. In the ninth and tenth in- ondarily adapted to a new purpose: to provide star, the wing pad twists over on the back (the additional protection for the lateral parts of same position is acquired in the antepenulti- their bodies. The beginning of the wing-discs mate moult of Orthoptera, by evolutionary and their migration dorsally and posteriorly convergence). Further changes, up to that in was found to be especially well expressed in the final nymphal instars, are mostly only the roaches. Ironically, this group has for a quantitative. long time been considered to be the bastion of According to Bocharova-Messner (’65) the the paranotal theory (Lemche, ’42; and nymphal wing pads of Ephemeroptera un- others). dergo a similar development, but because of Wing development in the crickets was simi- the compression of the number of instars, re- lar to that in roaches, but the wing-fold evagi- capitulation is less distinct at the beginning of nated first in the lateral position and only the ontogenetic series. The wing sack is omit- then migrated to fuse with the tergum. In ted and the wing evaginates as a narrow later- grasshoppers, due to embryonization of earlier al fold close and parallel to the tergum. Later, instars, wing development started in the em- it fuses with the tergum and combines with bryo and the wing fold was already present in the narrow posterior tergal fold to encircle the the first instar, as previously observed by tergum laterally and posteriorly. Starting in Tower (’03). about the sixth instar, the fold elongates suc- In all, Tower and Bocharova-Messner cessively at the posterolateral angle. Gradu- reached the same results: that the wings are ally it gains more and more resemblance to the in no sense a “dorsal backward prolongation of wing pads of neopterous nymphs, especially to the tergum,” but free lateral structures which, Plecoptera. In this way the mayfly nymphs for the mechanical convenience of the imma- not only become equipped with “paranota,” ture insects, are shifted in later moults to but also become “related” to Neoptera, on the another position and fused with the tergum grounds of the convergent external resem- (or tergal paranota if they are present). Tower blance of the older instars of both groups. How- (’03) was perhaps the first author to be con- ever, Neoptera were derived from paleop- vinced that the ontogenetic development of terous stock, but not from Ephemeroptera (see wing structures in Paleoptera and exop- sections IV, VI). terygote Neoptera was fully comparable with Observations on the development of wings that of the Endopterygota; this concept is in early instars of Hemiptera, Blattodea, presently accepted by many students of Orthoptera, Coleoptera and Lepidoptera were entomology. INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD 59

The fossil evidence, which will be discussed to uphold the paranotal theory. However, the in more detail in the next section; shows that hinges of pteromorphs in oribatid mites are all Paleozoic nymphs of Paleoptera and most simple lines of weakness and they show only primitive Neoptera have articulated and func- that any protruding lobes might become tional wings throughout their whole onto- movable through the attachment of near-by genetic development. This fact strongly sup- musculature. This movability of integumental ports Tower’s conclusion that the wings are evaginations also occurs in structures like free lateral structures. spurs. In mites, the pteromorphs have nothing to do with flight, but serve as protective The paranotal theory devices (if pulled in, the already smooth body In the currently quite popular paranotal becomes completely globular). On the other theory, also known under the spirited name of hand, the controlled gliding in butterflies, the “flying squirrel theory” (Muller, 1873- dragonflies, locusts and other insects, is ac- 1875; Crampton, ’16) the wings are derived complished on large wing planes, with from rigid, doubled, lobe-like expansions of sophisticated articulation and mostly with the thoracic terga, the paranotal lobes. Recent help of special locking mechanisms to hold the support for the paranotal theory has been wings outstretched. It does not prove the pre- given by Sharov (’661, Hamilton (’71-’72), existence of a solid tergal outgrowth, any Wootton (’761, and Rasnitsin (’76). more than does the gliding of an eagle “prove” Paranota are lateral expansions of the terga the pre-existence of a solid, spinal outgrowth which, in numerous arthropods, serve as pro- that eventually broke up into joints because of tection for the sides of the body and limbs. the eagle’s frequent gliding (!). They are described in trilobites, crustaceans, Indeed, flapping flight structures have Acarina, and myriapods. In insects, they are probably never evolved anywhere in the Ani- typically developed on the terga of Aptery- mal Kingdom, unless a suitable set of joints, gota. Paranota are primitive, may possess muscles, etc. were previously present and venation, and may even develop a simple preadapted for more specialized flapping func- hinge along a desclerotized line so that they tion. However, gliding is often used by ani- may become movable up and down to some ex- mals with flapping abilities as an energy-effi- tent (as the leg-protecting devices of galum- cient way of flight (typically by flying fish). nid mites). Paranota of silverfish strongly re- We have flapping flight alternating with glid- semble, in general morphology and trachea- ing flight in flying reptiles, birds, bats and in- tion pattern, those of immobilized wing pads sects. Contrary to this, the “gliders,” namely in older pterygote nymphs. The recapitulation squids, lizards, snakes, marsupials, and squir- principle, as well as these data of comparative rels, are restricted only to gliding flight, be- morphology, seemingly favor homology be- cause the primarily gliding planes do not need tween pterygote wings and thoracic paranota any “flapping” character to be effective. After of the Apterygota, if phylogenetic considera- an existing gliding organ has been perfected, tions are omitted. “natural selection would eliminate the indi- In the classical view of the paranotal viduals less apt at soaring. Hence, once a theory, the wings originated as follows: ini- soarer, always a soarer” (Grant, ’45). It is tially the protective thoracic paranota became therefore hard to believe that in insects the enlarged and acted first as parachutes in sophisticated flight apparatus developed from delaying descent; next as gliding surfaces; solid lateral extensions of the body. Through then as steering vanes; and ultimately as flap- the years, many efforts have been devoted to ping aerofoils (Wootton, ’76). This concept proving that insects could successfully glide seemingly finds support in the ability of some on small lateral “paranota.” Such an ability insects to glide and steer on wings oriented at cannot be reasonably doubted, as long as the an angle to the body, and in the morphology of insect body, or a simulation model, or any some oribatid mites. Woodring (’621, after a other body, do not violate certain aerodynamic detailed study of the hinged, movable, trache- laws. But this, clearly, does not furnish any ated and veined pteromorphs (paranota)of the evidence for a particular origin of the wings. oribatid mite Galumna eliminatus, saw a par- All conclusions on this matter are over- allel between the pteromorphs and insect simplified and mechanistic. “paranota,” which he believed to be precursors On the other hand, any flapping organ is of wings. He anticipated controlled gliding as bound to be very complicated and sophisti- a preadaptation to flying. All these data seem cated. It is generally believed among paleon- 60 JARMILA KUKALOVA-PECK tologists that a flight organ has to pass pads of all modern nymphs are not articulated through an intensive preadaptation period to, but are directly continuous with, the before it can be used for this function in an tergum; the haemocoel, nerves, and tracheae aerial environment. For instance, to become continue unobstructed from the body cavity preadapted for flapping flight the insect wing into the wing pads, and the latter thus seem to had to acquire a sufficiently large and thin form perfect postero-lateral outgrowths of the plane, supported by stiffened and corrugated tergum (figs. 3, 4). 2. The “proof” of the serial venation, an incipient rotating mechanism, homology was based on the similarity between and a coordinated set of flight muscles. There nymphal wing pads, prothoracic lateral ex- is an indication in the fossil evidence that all pansions, and abdominal lateral expansions, these characters might have evolved already because they show the same rigid and in the pre-flight wings (see following section unobstructed connection with the notum. 3. on origin of wing corrugation); and there is a The “proof” offered by the fossil evidence has convincing fossil record documenting that the been erroneously reported by paleontologists wings of pterygotes evolved from freely artic- (see below). Lateral lamellae on the palaeodic- ulated lateral appendages, as will be described tyopteran abdomen (here interpreted as in more detail below. marginal subcoxae, figs. 22-24) were generally It should be noted that soaring occasionally considered as paranota serially homologous to occurs in various insect orders. Among Paleop- wings. Prothoracic winglets of Paleodictyop- tera, the wings of dragonflies are in an elastic tera were viewed as “typical paranota” proven equilibrium (i.e., their placement is effortless- to be primitively continuous with the pro- ly maintained) when they are in the horizon- notum and forming its solid lateral out- tal position convenient for gliding (Neville, growths (see fig. 1 for an opposite view). Since ‘65). In Neoptera, the outspread placement of prothoracic winglets carry venation homol- wings has to be secured by various cuticular ogous to wings (fig. 141, the paranotal theory locking mechanisms (Neville and Weis-Fogh, was given powerful but false support (Ham- in Neville, ’65) acquired by adaptation. Thus ilton, ’71-’72). Wootton (’76) admitted that the locusts, the fly Chironomus and the lace- they might actually reflect the somewhat wing Chrysopa glide with locked fore wings, movable “steering vanes,” which are, accord- while the stag beetle Lucanus glides with ing to the paranotal theory, the hypothetical locked hind wings. Locking mechanisms are stage between solid paranota and articulated diverse and probably widespread. I believe wings. that the ability to use both soaring and flap- The ancestral insect “gliders” were recon- ping flight in Paleoptera is primitive and that structed as carrying on their thorax either early Pterygota, which had their wings in the three pairs of “paranotal” lobes which looked paleopterous position (fig. 46B), were able to like prothoracic winglets of Palaeodictyoptera fly with alternating periods of soaring and but were considered to be immobile (Zalessky, flapping. However, the evolutionary trend was ’53) or which looked like nymphal wing pads of towards improving the flapping, and soaring modern roaches and were spread permanently was retained as an option which every flying obliquely backwards (Sharov, ’66). The “para- animal possesses to some degree. Effortless nota” on the abdomen were anticipated as gliding was bound to be very important, espe- similar to the thoracic ones but smaller. The cially in an early evolutionary period when timing of gliding and wing origin were then flight was imperfect and the wing beat slow, explained by the synchronous occurrence of because it is energetically the most economi- high trees at the end of the Devonian (Hock- cal way to gain height and to disperse. In con- ing, ’57), from which the insects voluntarily trast, the locking mechanisms in Neoptera are jumped or were knocked off by wind. clearly secondary adaptations for regaining soaring which was lost when the wings had de- Fossil and comparative-morphological veloped the ability to flex backwards. This evidence new adaptation evolved independently in The fossil record confirms none of these diverse groups to conveniently support either “facts” that “support” the paranotal theory. pair of wings. In fact, it provides evidence to the contrary. In The paranotal theory was constructed upon the last decade, numerous nymphs of gen- three basic points: 1. The “proof” offered by eralized Paleozoic orders have been described ontogeny was seen in the fact that the wing and these were found to have articulated and INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD 61 functional thoracic wings: Ephemeroptera by were rather peculiar and heavily sclerotized, Kukalova ('68) ; Megasecoptera by Carpenter and the functional efficiency and mobility of and Richardson ('68) ; Palaeodictyoptera by their wings were reduced by this specializa- Sharov ('66, '71a,b), Wootton ('721, and by tion (they presumably avoided predators by Kukalova-Peck and Peck ('76); Protorthop- pressing against the substratum), (figs. 22, tera by Sharov ('57a, '66) and Miomoptera by 24). I studied fossils of the nymphal wings of Sharov ('57b). Independently articulated ab- Ephemeroptera, Megasecoptera, Palaeodic- dominal wings have been lost in most orders tyoptera, various Protorthoptera, and Blat- except in some Protorthoptera (fig. 351, (Car- todea, and closely examined the way in which penter, '35), and Ephemeroptera (Kukalova, they are attached to the tergum. The articula- '68). All these nymphs, some 300 million years tion and degree of mobility varies in different before the Recent, had freely articulated groups of both Paleoptera and Neoptera. The wings even in the youngest instars (Kukalova, most primitive condition, with a clearly inde- '68) (figs. 6, 22, 24, 25, 28, 30, 31, 33, 35, 47, pendent attachment and the greatest ma- 48). Modern juveniles descendent from noeverability, is found in the Ephemeroptera Paleozoic lineages (fig. 46A: Recent) then can (figs. 28, 30) and the Megasecoptera (fig. 31). not be morphologically more primitive be- In Protorthoptera the condition varies from cause of their possession of functional struc- completely independent wings (figs. 35, 47, tures that are like "paranota." Clearly, the ar- 48), known also to Sharov ('57a,b, '66), to wing ticulated wings of Paleozoic nymphs are prim- pads fused completely with the thorax. The itive, while the immobilized wing pads fused last, a specialized condition, is characteristic with the tergum in modern nymphs are for blattoid Protorthoptera and especially for derived. the Blattodea which were the first to attain It is concluded that all body segments in the typical morphology of modern nymphs. Paleozoic nymphs carried wings which were There is hardly any doubt that the trend to primitively movable. This movable attach- repress the articulation and to immobilize the ment was carried over from the immediately wing pads started very early in Paleozoic preflight Pterygota in which yet undis- nymphs and has since proceeded in all lines, covered articulated pro-wing structures were but at different rates. However, the fossil evi- situated along the whole body and were dence of primitive movability is convincing, involved in active motion beginning with the especially in Ephemeroptera: about 100 young nymphal instars. The immobilizing of minute nymphal wings were found in the the thoracic and the loss of the abdominal lower Permian deposits of Oklahoma (F. M. wings in the nymphs of some Pterygota was Carpenter, personal communication, and per- already underway in the Upper Carboniferous sonal observation) which were broken off (figs. 22, 24) and has proceeded ever since in along the hinge line identically as were the all major lineages. wings of the adults. A similar phenomenon is If the movability and articulation of Paleo- known also in numerous Paleozoic Megasecop- zoic nymphal wings is known to paleoentomol- tera. This provides convincing evidence that ogists, how is it then possible that Sharov in the ontogeny of primitive Paleozoic lines of ('661, Wootton ('72, '76) and Rasnitsin ('76) Pterygota even the youngest nymphs could defended the paranotal theory? flap their wings. Sharov's support for the paranotal theory Both Wootton and Rasnitsin considered the stemmed from an error in classification. He function of the deep groove (previously de- believed that two isolated, chitinous, veined, scribed by Sharov, '71a,b) along the base of the telsonal plates (uropods) of a Devonian crusta- paleodictyopteran nymphal wings (figs. 6a-c, cean, Eopterum devonicum, were the wings of 23,241, and independently concluded that it is an ancient pterygote (Rohdendorf, '72). a simple line of bending. They compared this Hypothetical paranota in the transitional structure with the groove along the wing base stage of "steering vanes" would probably have in some nymphal Neoptera, and presumed looked similar to these plates, if the paranotal them to be homologous. This "homology" was theory were valid. believed to support the paranotal theory. Wootton ('72, '761, and Rasnitsin ('76) stud- However, this conclusion is based upon a ied only the nymphs of Palaeodictyoptera and misinterpretation. The deep groove along the did not have the opportunity to examine other wing base in palaeodictyopteran nymphs is Paleozoic Paleoptera. Some of these nymphs the paranotal sulcus (figs. 45A,B: pa), which 62 JARMILA KUKALOVA-PECK is part of the sophisticated articulary region in Recent forms this hinge-vestige has mostly of the functional wings. This is typical for the disappeared. However, in some Recent pray- primary pterygote hinge of the paleopterous ing mantises the rudimentary cuticular, cres- type, which was straight and composed of cent-shaped hinged base is quite distinct (fig. serially arranged pteralia (as documented 18). Further proof of the serial homology in here in section I11 on Origin of wing articula- tracheation is given in the prothoracic wing tion).The groove, along with the presence of lobes of mutated Blattellagermanica, by M. H. pteralia (figs. 6. 22; Wootton, '72: fig. 3b; Ross ('64). The prothoracic tracheal wing-loop Rasnitsin, '76: figs. la-c) indicates the pres- (transverse basal trachea of Whitten, '62) of ence of an articulary region in very young these nymphs not only bears marked resem- nymphs of Palaeodictyoptera which alone pro- blance to that of the mesothoracic wing, but vides a uniquely strong argument against the also is connected to the genuine (though tem- paranotal theory. The shallow grooves along porary) prothoracic spiracle, which occurs for the base of the neopteran wing-pads, on the a short time in early instars (otherwise, the other hand, are either the mesa1 limits of the prothoracic spiracles in all adult living insects movable wings, or the lines of fusion between are completely missing). the wings and the tergum along the anal area. In any case, whether the prothoracic wing- The evidence of the fossil record as to the lets are preserved in the form approaching "immobility" of prothoracic lobes is simple: that of pre-flight wings as perhaps is the case there are no primitively immobile prothoracic in Palaeodictyoptera, or whether they had lobes which could logically be homologous been mechanized for some kind of forward with wings (figs. 14-21). Instead, they were motion (terrestrial or underwater) as in some primitively movable and are now secondarily undescribed fossil material, or whether they immobile. Traces of former mobility in pro- had lost mobility and served to protect the thoracic lobes can be detected in both fossil head and legs, they are all homologous to and Recent insects. Evidence of positively wings and primitively were articulated to the movable prothoracic winglets in some Palaeo- prothorax. dictyoptera is presented in fig. 1 (both Genuine prothoracic winglets should not be winglets are separated from the pronotum and confused with true prothoracic paranotal superimposed). Also, a certain movability of lobes, which exist on the terga of brisletails lobes in some Protorthoptera is not excluded and silverfish (Apterygota), or with narrow (Carpenter, '50, '66: plates 4, 5). Prothoracic lateral notal extensions that occur in some lobes of most adult Protorthoptera are juvenile and adult pterygotes. Also, protho- immobile and protective (fig. 16), and occa- racic lateral extensions present in many sionally carry sensillae (fig. 17) similar to Hemiptera are not equivalent to wings, be- those of some modern insects. However, in cause they are well behind the pleural ridge, undescribed material in my collection, there at the dorsal end of which the wings would be are several nymphs of plecopteroid Pro- expected to articulate. The wing-derived pro- torthoptera that might possibly have had thoracic lobes are recognizable on the basis of movable prothoracic wing pads (fig. 35). their pleural suture which is roughly oriented Paleozoic adult and nymphal Ephemeroptera towards the former location of the wing's ar- from the Lower Permian have membranous ticular region. prothoracic winglets (figs. 15, 28), with rem- nants of venation and a crescent shaped Summary of evidence against the vestigial hinge. In undescribed material from paranotal theory Mazon Creek, Illinois (Upper Carboniferous, The articular attachment of wings in all in the Field Museum, Chicago) I have seen a primitive Paleozoic nymphs leaves no doubt paleopterous nymph with three pairs of that solid paranota engaged in gliding did not thoracic wings in a rowing position, equal in come first in the evolution of flapping insect size and with a mechanized venation pattern. wings. In fact, the adaptive trend was exactly Recent prothoracic winglets in mayfly the opposite: the nymphal wings lost their nymphs were described by Ide ('36) and are movability by fusion with the tergum, de- known in Dolania (Tsui, personal communica- veloped a thickened integument reinforced by tion). In Paleozoic roaches (figs. 19-21), the cuticular rugosities of various kinds, and thus crescent shaped articulation of the wing lobe finally came to be convergent with paranota. with the prothorax is clearly indicated, while The function of these changes was to protect INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD 63 tender wing tissue (and sometimes the legs) folds of the tergal margin. Hence, they are ex- and to streamline the body (compare figs. 29 pected to be primitively continuous with the and 30). tergal plate and well sclerotized, besides being In the past, the comparison between the doubled. In primitive Paleozoic insects, how- thoracic wings and the lateral margined ab- ever, the lateral parts of the abdominal seg- dominal expansions, generally considered to ments are separated by a suture which is often be paranotal lobes, has been the strongest oblique (figs. 22-24: SCX) ; under glycerin argument in favor of the paranotal theory, these fossilized “paranota” become trans- and in many discussions has been the decisive parent and are obviously less sclerotized and observation. However, the interpretation that pigmented than the neighbouring abdominal all abdominal lateral expansions in Pterygota terga. Consequently, they can hardly repre- are derived from the terga is doubtful, as sent solid, doubled tergal lateral outgrowths. shown in following text. More probably, they are pleuron-derived According to the fossil evidence, the structures, perhaps margined subcoxae. vestigial abdominal wings and legs were prim- It should be noted that, within the paleop- itively present on all abdominal segments of terous orders, the occurence of the abdominal both nymphal and adult Paleoptera and Neop- wings, legs, and margined “lateral lamellae” tera (figs. 46A,B). In Paleoptera, articulated (however they are interpreted), excludes the abdominal wings are preserved in the nymphs possible origin of wings from these respective of mayflies (fig. 25A), and are sometimes lateral lamellae. This conclusion is, of neces- noticeable as vestiges in mayfly adults sity, valid for all Pterygota with the assump- (Birket-Smith, ’71: fig. 1A). In Recent juve- tion that: 1. the thoracic and the abdominal nile Ephemeroptera all sclerites of each ab- segments in insects are serially homologous, 2. dominal segment are fused into a ring and the paleopterous Pterygota are ancestral to are discernible only with difficulty. Their the neopterous Pterygota. arrangement, nevertheless, is homologous In Paleozoic Neoptera, the abdominal wings with that of the pterothoracic segments: the have been found so far only in some immature tergum, the wing (a gill-plate, articulated be- (Carpenter, ’35) and adult (Kukalova, ’64: fig. tween the tergum and the subcoxa), the 47) plecopteroid Protorthoptera and in addi- (margined) subcoxa, the coxa (to which is at- tional protorthopterous nymphs from the tached the leg-derived gonostylus), and the Lower Permian of Kansas (figs. 25B, 35, 47, sternum (Snodgrass, ’35: fig. 150). This in- and undescribed material). Vestigial abdom- terpretation of the abdominal segments is inal legs are present as diverse styli and cerci probably valid for all fossil and living Paleop- in many Neoptera, and most notably form the tera. In some Paleozoic adult Diaphanop- gill-legs (tracheopods) in dobsonfly and sisyrid terodea (undescribed material from the L. larvae. It is therefore very probable that the Permian of Czechoslovakia), and some living abdomen of the most primitive Neoptera was dragonfly nymphs (Calvert, ’11; Corbet, ’62; very similar to that of Paleoptera and carried Matsuda, ’76: p. 134) vestigial legs are at- both wings and legs on each segment. The tached to the abdominal coxal region and thus wings have usually been lost without a trace. help in its identification. It is believed here However, in blattoid orders (both extant and that the extended sides of the abdomen (also extinct) and perhaps also in other orders, called lateral lamellae) of all immature and there is another possibility to consider: that adult Paleoptera, are formed by the margined the abdominal wings might have become fused subcoxae and not by the “paranota,” as fre- with the edge of the tergum in the same way quently anticipated. This interpretation, for- as did the nymphal thoracic wings, and per- mulated first by Borner (’081, has been based sisted there into the adult stage. This alterna- upon the serially homologous position and the tive possible interpretation is inspired by the adjacent musculature of the abdominal sub- fact that the Paleozoic blattoid lineage was coxae in living Ephemeroptera (fig. 25A). The the first to acquire a modern nymphal mor- fossil record gives support to this idea in the phology and the first to develop the metamor- morphology of abdominal “paranota” in primi- phic instar. This early evolutionary event tive Palaeodictyoptera and Megasecoptera might have perhaps heightened the chance from the U. Carboniferous (Museum d’His- that all wings along the body undertook the toire Naturelle, Paris, ’77, personal observa- same process of fusion with the edges of their tion): Paranota are supposed to be lateral respective terga. If this is true, the marginal 64 JARMILA KUKALOVA-PECK parts of the nymphal prothorax, the ptero- and apomorphic characters of venation. The thorax, and the abdomen in roach-related “archetype venation” models of Comstock- orders might in reality be serially homologous, Needham (1898), Bradley (’391, Snodgrass as assumed by the paranotal theory. At the (’35) and their numerous followers do not, by same time, they are by no means derived from any means, reconstruct a primitive venation. tergal (paranotal) expansions. For that reason they were frequently chal- It seems that the notal lateral extensions lenged by paleoentomologists (see Sharov, ’66, were primitively either small or absent in for summary). Some designations of veins, ancestral Paleoptera and that they stayed used occasionally by some present authors, are primitively small or absent also in early de- only typologically based and cannot be used scendent Neoptera. The features described as for broader comparisons and homologization; abdominal “paranota” or “paratergites” in examples are postcubitus (Snodgrass, ’35),pli- Hemiptera might be, at least in some cases, in- cal veins (Forbes, ’32, ’431, and plical and em- terpreted as margined pleura which grew pusal veins (Hamilton, ’71-’72). together with the terga. The problem of the The primary role of blood channels (rather pterygote lateral abdominal region needs deep than that of tracheae) for a determination of comparative study in all major lineages, in- the venation was suspected by sulc (’111, cluding the varied position of the spiracle and Marshall (’131, Kuntze (’35), and Ross (’36). of the pleural membrane. However, the primi- This concept has been recognized and sup- tive small size or absence of notal lateral ex- ported by several authors using the ap- pansions in earliest pterygotes seems to be proaches of histology, experimental teratol- essential for the origin of wings, and to be phy- ogy, ontogenetic analysis, comparative mor- logenetically more sound. It is also in agree- phology, and circulatory physiology (Tower, ment with fossil evidence and serial homology ’03; Holdsworth, ’40, ’41; Henke, ’53; Smart, in primitive Recent insects. ‘56; Whitten, ’62; Leston, ‘62; Arnold, ‘64). To summarize the various possibilities, The idea has similarly been supported by then, the Pterygota may have been derived paleoentomologists, as in many papers by Till- from an apterygote stock (1) in which the yard, Martynov, Carpenter, and Sharov. Yet, paranotal lobes were absent or repressed or, almost unbelievably, in the most commonly (2) in which they became reduced as the wings used entomological textbook in North Ameri- continued to increase in size or, (3) in which ca, Borror and DeLong (editions from 1954 to the primary absence of paranotal lobes per- 1976) and in some other recent textbooks, the haps stimulated the development of the wings. venation of Odonata is interpreted according to the “pretracheation theory.” Consequently Pretracheation theory of Comstock-Needham the “media” comes out “crossing” the “sector Few works have influenced entomology as radii,” which is never the case among the deeply as has “the Wings of Insects” by Com- Pterygota and creates the false impression stock and Needham (1898-1899) and again by that the dragonflies are thus unique. Comstock (’181, in which the authors homol- The precursors of the veins in the nymphal ogized wing venation between insect orders wing pads are the lacunae, free spaces which (for the more complete analysis and historical are surrounded by the spongy columnar epi- account see Carpenter, ’66). But however dermal cells (figs. 3, 4). According to Holds- much the work contributed in its time, it also worth (’40,’411, tracheae andnerves grow into introduced several errors, which are as fol- these channels only after their pattern has lows: interpreting the wings as if tracheation been established. The veins are secreted by the determines the position of the veins; the epidermal cells through deposition of cuticu- assumption that the tracheation in nymphal lar material above and below lacunae only at wing pads recapitulates the venation of adult the final nymphal/adult moult. During ancestors; the failure to recognize corrugation ontogenesis, the position of tracheae may or and richly ramified venation as primitive and may not reflect the future venational pattern. phylogenetically important features; and the Wing tracheae may increase in number at overlooking of the crucial significance of each ecdysis, and new tracheae may grow out fossils for the detection of missing or fused into areas deprived of oxygen (Wigglesworth, veins and for clarifying the venation pattern. ’54; Locke, ’58; Smart, ’56); tracheation may All these misinterpretations were closely also be influenced by temperature (Henke, linked, and have confused some plesiomorphic ’53). According to Whitten (’621, each instar INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD 65

(including the pupal stage), possesses its own was independently tracheated from its own tracheal system which may more or less differ pair of spiracles (Snodgrass, ’35). In the em- from that of the next instar and from the bryo, the tracheae start intrasegmentally, as adult stage. The tracheal pattern is not paired ectodermal invaginations. This seg- necessarily homologous between instars, be- mental condition is well expressed in primi- cause new additional tracheal branches may tive apterygote insects (machilids). In the be formed and old ones discarded. However, pterygote body, the complicated tracheal net- there is still a degree of stability and if no work (longitudinal anastomoses and trans- changes occur in the areas to be served, the verse commissures) resulted from connections tracheae probably follow a constant develop- of the primary segmental tracheal systems, at mental pattern (Landa, ’48; Henke, ’53; Whit- first probably to give more efficient aeration. ten, ’62). According to Whitten (’621, at a Accordingly, structures like legs receive addi- generic or family level, wing tracheation in tional air supply from the spiracle on the fol- some insects is stable enough to be helpful in lowing segment; the posterior part of the the study of the venation pattern. Attempts to wings is served by a side branch which diver- deduce phylogenetic trends on the supraor- ged from this secondary leg-trachea. dinal level have, however, been unsuccessful. Contrary to the above, tracheation in It should be noted that the particular Ephemeroptera is restricted in each somite to tracheae, which serve the wing, never “mi- that of its own spiracle. This condition is most grate” or “fuse,” as has been erroneously likely to be close to the archetype stage, and brought forward by Comstock and Needham thus to be more primitive than that of the other (1898-1899) (this occurs solely in the tubular Pterygota (for more detailed documentation venation). see Weber and Weidner, ’74).Previously, some In almost all insects, each fore and hind doubts were cast on this obvious conclusion. wing is served by two tracheae (Whitten, ’62): These doubts stemmed mainly from several the anterior trachea, which supplies oxygen to reports of “residual remnants” of posterior the costo-median venation; and the posterior tracheal branches in some mayflies (Kristen- trachea, which supplies the cubito-anal vena- sen, ‘75, for discussion). However, these data tion. The anterior trachea arises from the re- must have been mistakenly observed for the gion of the spiracle located anteriorly to the following reason: Whitten (’62) showed that wing in question, the posterior trachea from whenever anterior and posterior alar trachea the spiracle located posteriorly (since the come into contact, there is a structure called prothoracic spiracle has been completely lost tracheal nodus. Thus, the tracheal segmental in all living adult insects, the mesothoracic systems do not fuse, as is often erroneously spiracle became anterior and the metatho- stated, but connect at tracheal nodi which racic became posterior with regard to the fore again disconnect at ecdysis. Since such a wing; the hind wing is supplied from the nodus is missing from the alar tracheal sys- metathoracic and the first abdominal spira- tem of Ephemeroptera, each system moults cles). The dividing line between two tracheal with, and consequently belongs to, only one metameres (tracheations of primary body seg- somite. ments) runs into the wing between the anteri- Another question is the timing of the inva- or and posterior trachea. As shown by Whitten sion of the posterior alar trachea into the (’621, both pairs of alar tracheae moult with cubito-anal system of Pterygota. Segmental their respective spiracles, i.e., within their tracheation is present in primitive Apterygota two different segments. The only exception and must have been present in the paleopter- are the Ephemeroptera in which all veins, in- ous ancestors of Paleoptera and Neoptera, be- cluding the cubito-anal system, are served cause it occurs as relic structure in modern only by the anterior trachea from the anterior Ephemeroptera. We have no way to estimate spiracle. Whitten (’62) correctly concluded when and how many times occurred the inva- that the cubito-anal tracheal branches in sion of posterior trachea into the cubito-anal Ephemeroptera are not homologous to those of veinal system. However, it is probabIe that at any other insect order. The question is least in Odonata and Neoptera the double alar whether this condition is primitive or derived. tracheation resulted independently, from par- Deductions should be built upon the fact allel evolution. that in the primitive stage, each insectan The fossil record is not very helpful in docu- somite (metamere, primary body segment) menting the events of tracheation, because 66 JARMILA KUKALOVA-PECK the crucial basal tracheal branching is within involved. The flap flattened, increasing its the thorax and is not preserved. However, ratio of surface area to volume, and at this some results may be drawn from the venation stage it started to help with forward locomoto- of Paleozoic nymphs which can be compared ry movement. Gradually, the leg muscles with the tracheation of old modern nymphs came to coordinate the motion of the legs and and metamorphic instars (true tubular vena- flaps. The evolutionary process finally re- tion of Paleozoic nymphs corresponds to the sulted in the formation of a mobile, flattened invisible blood lacunae in the wing pads of appendage with a high frequency of beating modern nymphs, which in both cases hold the which was helpful in rapid running, and had tracheae). It should be noted that the veinal the potential of later becoming mechanized pattern near the wing base of Paleozoic may- for flying. This detailed resume of Bocharova- fly nymphs (fig. 2) closely resembles the Messner's ('71) paper is given because her in- tracheation pattern in primitive modern teresting spiracular flap theory is practically nymphal mayflies, such as Siphlonuridae. If unknown to most English-speaking ento- this cannot render the proof that the alar mologists. tracheation of some Ephemeroptera stayed This hypothesis brings several intriguing almost unchanged since the Paleozoic, it is at aspects to our attention, such as: the possi- least indicative of this conclusion. bility of a primary exploration-inspection role To summarize present knowledge: tracheae of the wing evagination; the possible involve- serve the wings by delivering oxygen and de- ment with regulating the closure of the velop in the pattern established by the inci- atrium and thus gas exchange in the trachea; pient venation, but tracheae never indicate and the possible participation of the pre-wings the course of the veins. In some insects, the in running. If the evagination first formed a tracheation is quite stable and may turn out spiracular flap, this would probably be a new to be helpful, especially in older instars, in un- structure, analogous to a flattened spur. The derstanding venation on an infraordinal level. current fossil evidence neither proves nor dis- However, since tracheae never fuse and never proves the spiracular flap theory, but there migrate (but veins do), the terminology and are at least two features which might be in- principles used for venation are not fully ap- terpreted as supportive: First, Permian may- plicable to tracheation, as is often erroneously fly nymphs, which were secondarily aquatic, practiced. Tracheation inside of nymphal typically had slender, long, cursorial legs (fig. lacunae does not recapitulate the macroevolu- 28) with long, 6-segmented tarsi. Similar or tionary events of the wing venation; this can only slightly different (shorter) legs and tarsi be found only in the venation of fossil insects. were also present in Palaeodictyoptera and many other generalized Paleozoic insect Spiracular flap theory orders. It thus seems quite likely that early Bocharova-Messner ('71) considered the (terrestrial) pterygote legs might have been possibility that wings originated from integu- well adapted for running. Second, it is impor- mental evaginations which at first served as tant from an evolutionary viewpoint that spiracular flaps. Data for this hypothesis were ancestral (presumably semiaquatic) Ap- drawn from her study of wing development in terygota lacked a spiracular regulatory mech- Odonata (Bocharova-Messner, '59) (fig. 36). anism for the control of respiratory water loss. She suggested that the small spiracular flap Control of body water content is extremely first achieved mobility by acquiring muscular important for the survival of terrestrial (and and sensory mechanisms to aid in respiration. especially of flying) insects. Therefore, it is The primary function of the integumental almost certain that some kind of water regula- evagination above the spiracle was tactile and tion mechanism must have originated at exploratory. Later, a larger fold developed to about the same time as the wings, if we protect the spiracle and to create a chamber assume that the early pterygotes originated around it. With time, the fold enlarged and on dry land. became mobile, perfecting the protective Bocharova-Messner's spiracular flap theory function. Eventually it became large enough seems debatable on the basis of spiracular dis- to serve as a ventilating mechanism for the tribution. The largest number of spiracles tracheal system. With this newly acquired found in modern adult insects is ten pairs: two function, the mobility of the fold continued to thoracic and eight abdominal. The first spira- improve and the respiratory muscles became cle is often on the prothorax, but is meso- INSECT WINGS, METAMORPHOSIS. AND THE FOSSIL RECORD 67 thoracic in origin. The true prothoracic spira- of the thoracic wings of mayfly adults with cle was lost. When less than ten functional the abdominal gill-plates of mayfly nymphs, spiracles are present, the “non functional” rather than with the legs (Snodgrass, ’35; ones persist and open at the time of ecdysis Imms, ’64) or leg exites (Birket-Smith, ’71): and permit the cast intima to be shed (Chap- 1. Mayfly nymphal gill-plates are segmen- man, ’69). How does this number and position tally arranged, articulated, and moved by sub- of existing spiracles agree with the fact that coxo-coxal muscles (figs. 26,381. They are very some fossil insects have three thoracic wings different from the typically soft and floppy and that the maximum number of abdominal filamentous gills of other aquatic juveniles, winglets so far documented in Neoptera is ten which occur without a definite arrangement (in juvenile plecopteroid Protorthoptera, fig. and which lack musculature. The main func- 351, and in Paleoptera is nine (in juvenile tion of gill-plates is primitively 2-fold: to drive Ephemeroptera, fig. 28)? currents over the tracheated surfaces, and to According to Snodgrass (’351, spiracles have render aid in locomotion. For the last, the been found on 14 insectan segments; they are leading margin is often strengthened as in the second maxillary segment, the three thoracic wings (fig. 25A: am). thoracic segments, and the first ten abdom- 2. Mayfly nymphs never develop gill-plates inal segments. Wheeler (1889) detected 12 on the thorax or head, but they do develop reg- spiracles (3 thoracic and 9 abdominal) in the ular filamentous gills there. embryo of Leptinotarsa decemlineata. This ob- 3. In Paleozoic mayflies gill-plates were servation was later repeated and confirmed by present on all nine segments of the abdomen Tower (’03). According to M. H. Ross (’64) true (figs. 28, 30). The leg-derived gonostyli prothoracic spiracles may also occur in mu- (claspers) in all mayflies are attached ven- tants. In newly hatched nymphs of mutated trally to the ninth segment; the vortex-like Blattella germanica, these appeared anteri- traces of nymphal abdominal wings, found in orly on the prothorax, close to the cervical living adults by Birket-Smith (’71: fig. lA), membrane. Even though the openings quickly are located more dorsally, in a position serially disappeared, their position was marked as a homologous to the thoracic wings. meeting place of a number of tracheae, like 4. Mayfly gill-plates are articulated be- those of the permanent spiracles. Consequent- tween the subcoxa, and the tergum (fig. 25A) ly, ancient insects probably had a pair of spira- like thoracic wings. This location is main- cles on each body segment, as was previously tained, even if the gills are completely dorsal deduced by Snodgrass (’35). because of the lateral, expanded, and mar- In his detailed work on larval wings, Tower gined subcoxa (Crampton, ’16, regarded this (’03) repeatedly found incipient wing-discs in seemingly “tergal” position of the gill plates Coleoptera, Lepidoptera, Orthoptera, Blat- as strongly opposing their homology with todea, and Hemiptera in exactly the same po- thoracic wings). sition, close to and above the spiracle. Finally 5. In the gill-plates of modern mayfly he became convinced that “the wings are de- nymphs, there are often remnants of a true rived in some way from the tracheal system.” venation (Woodworth, ’06; Needham et al., This statement might be also interpreted as ‘35; Wigglesworth, ’76; Landa, personal com- support for the “spiracular flap theory.” munication) as in thoracic wings (compare (figs. 25A and 28). Moreover, in Paleozoic Stylus theory mayfly nymphs (fig. 281, the venation of gill- Wigglesworth (’73, ’76) has introduced a plates serially repeats the whole (but simpli- novel hypothesis suggesting that wings origi- fied) venation of the thoracic wings. This evi- nated from the coxal styli of Apterygota. He dence of serial homology in venation pattern assumes that the thoracic wings are homol- should be regarded as important. ogous with the abdominal gill-plates of mayfly 6. In their ontogenetic development, gills nymphs and with the abdominal styli of begin to occur in the second or third instar. apterygotes, which he considers to be serially According to Durken (’07, ’231, they evaginate homologous with the coxal thoracic styli of from the body wall (fig. 38) as do thoracic Archaeognatha. This homologization is dis- wings. He considers the gill-plates to be new putable and is contradicted here. However, structures which are not derived from the there are several phenomena discussed below, terga. After evagination, the gills migrate which do favor Wigglesworths homologizing closer towards the posterolateral angle of 68 JARMILA KUKALOVA-PECK the tergum. The same process of migration penter, '351, but I have seen other fully winged takes place in the incipient thoracic wings protorthopterous nymphs of various types, of modern generalized nymphs (fig. 361, from the same locality (figs. 35,481. In opposi- (Bocharova-Messner, '59, '65; Tower, '03). The tion, modern Neoptera do not show appen- gill-plates might be doubled, but both lobes dages equivalent to the abdominal wings. stay attached to the single common base. According to Zwick ('731, the ventrolateral 7. According to Snodgrass ('35, '52) the gill- segmented abdominal gills known in some plates are supported by two lateral sclerites, modern Plecoptera (Eustheniidae, Diamphip- located between the tergum and the sternum. noidae, Pteronarcidae, and few primitive Per- They are articulated to the dorsal sclerite, lodidae) are situated below the spiracular scar while the muscles extend between the gill- and therefore cannot be homologous to wings; base and the ventral sclerite (figs. 25A, 38). If neither are they homologous to legs, because we agree with Borner ('08) that the dorsal they develop independently from abdominal sclerite is the subcoxa, and with Wigglesworth limb buds (Miller, '40). Thus, there is evidence ('76) that the ventral sclerite is the coxa, then in Paleozoic insects, but no readily apparent the muscles moving the gills are the subcoxa- proof in modern insects, that the vestigial ab- coxal muscles. The same muscles in the thorax dominal wings were primitively present on the are stretched between the wing base and coxa abdomens of Neoptera. and serve as direct flight muscles. The serial homology between (1) the wings 8. The abdominal wings (gill-plates) of and (2) the abdominal styli of Apterygota and mayflies are articulated to the subcoxa and some larval Pterygota (Megaloptera, some are always located above the level of the Neuroptera, Coleoptera and Zygoptera), as (obliterated) spiracle, like all pterygote tho- proposed by Wigglesworth ('761, cannot be racic wings. On the other hand, the leg-de- accepted. In Pterygota, the thoracic wings are rived gonostyli, styli, cerci, and gill-legs always found above the spiracle (i.e., dorsally (tracheopods) of some nymphs are articulated at the subcoxa) while the legs are always un- to the coxae (Snodgrass, '35; Smith, '70a,b), der the spiracle, i.e., within the coxal region always below the level of the spiracle. This (Snodgrass, '35). The same conclusion has shows the duality of the abdominal appen- been confirmed by Landa ('48) on the basis of dages in Paleoptera, as well as the pronounced tracheation: his section through an abdominal serial homology of all body segments, which is segment of a mayfly nymph shows the inter- frequently unexpected and thus overlooked. mediate position of the spiracular trachea be- 9. To summarize the data: the gill-plates of tween the vestigial leg- and gill-plate tracheae mayflies are segmentally arranged abdominal (fig. 40). Moreover, the telopodite-derived appendages, always located above the spira- body appendages, legs, styli, gill-legs (tra- cle, which evaginate and develop very much cheopods), gonostyli and cerci, are never like the thoracic wings; they are also provided known to migrate above the level of the spira- with true venation, articulated between the cle in order to articulate or fuse with the subcoxa and tergum, and moved by the sub- tergum, as is routinely done by incipient gill- coxo-coxal muscles like thoracic wings. plates and wings. Following workers (see Landa, '48, for full Even though the position of mayfly gill- citations) believed that the gill-plates are plates in relation to the spiracles cannot be ex- serially homologous with wings: Gebenbauer ternally observed (the spiracular openings (1870), Lubbock (18731, Brauer (18821, Pal- were lost when ephemerid nymphs switched to men (1887), Simroth (18911, Voss ('031, and apneustic respiration) it is neverless well Woodworth ('06). More recently, the same known. As described by Durken ('23) and Lan- view has been taken by Wigglesworth ('73, da ('48), the anlage of the future adult spiracle '76) and Matsuda ('76). An identical conclu- is clearly indicated by the tracheae, and the sion was reached here on the basis of the fossil gill-plates are always located above the evidence. spiracular level, as shown in figs. 37, and 40. Abdominal wings are not restricted to the According to Birket-Smith ('71: fig. 1A) the Ephemeroptera, but they occur also in some abdominal wings are indicated in the adults of extinct Neoptera, in young as well as adults. primitive Povilla adusta by a vortex-like So far, they have been described in the trace. This is also located above the spiracular nymphs of plecopteroid Protorthoptera from level, while the gonostyli in the same species the Lower Permian of Elmo, Kansas (Car- are under the spiracle. INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD 69

In the modern literature, the abdominal thoptera from Elmo, Kansas, is in preparation. styli, gonostyli, and cerci are interpreted In Wigglesworth's ('73) hypothesis insect either as coxal exites or as reduced legs. Late- wings are derived from the coxal styli of ly, Smith ('70b, '76: XV. Int. Congr. of apterygotes, so that in ancestral pterygotes Entomology) considered that maxillary and the basal parts of the coxal limb bases (i.e., labial palpi, gonostyli, abdominal styli and subcoxa: Snodgrass, '35) of the thorax became cerci are serially homologous with complete incorporated into the thoracic wall to form the telopodites (legs). He believes coxal styli of pleuron, while the sites of articulation have apterygotes to be coxal endites that have migrated dorsally to the margin of the notum rotated somewhat outward, i.e., they are not (Wigglesworth, '73, '74, '76). According to homologous with abdominal legs. There is Smith ('76: XV. Int. Congr. of Entomology) some fossil evidence for the primitive arrange- the primitive apterygote subcoxa was already ment of the leg-derived abdominal appendages differentiated from the coxa and formed an in Pterygota: adult terrestrial Diaphanopter- annulus, as on some head appendages and on odea (extinct Paleoptera) in my undescribed the meso/metathoracic legs of fossil Monura material from the Lower Permian of Czech- and modern Archaeognatha. It is therefore oslovakia have a series of segmented styli on probable that the subcoxa was previously free the abdomen. Probably the segmented abdom- from the coxa before it became incorporated inal vestiges of legs were inherited from Ap- into the pleural wall. Since the coxa remained terygota and were primitively present as a associated with the telopodite, the subcoxa of plesiomorphic feature in all abdominal seg- the earliest Pterygota was bound to be in the ments of early Pterygota. Many of these leg- way of any potential migration of the coxal derived appendages were carried over to living stylus. insects and fulfill different functions. From the paleontological viewpoint, Wig- In the modern insects, vestigial abdominal glesworths ('73) hypothesis would be more legs are randomly preserved as cerci, styli, credible if the annular subcoxa itself bore a tracheopods (gill legs), and gonostyli through- movable appendage (exite) before it became out the pterygotes (the larval prolegs of part of the pleural wall (subcoxal appendages holometabolous insects are not serially homol- are known in some primitive Crustacea and ogous with the legs: see review in Hinton, '55). Chelicerata). The similarity of the pleuron in They are especially long and conspicuous in some Apterygota (Thysanura) and Pterygota aquatic juveniles of corydalids, sisyrids, and can most probably be explained by parallel probably in some damselflies, in which they evolution. It should be noted that the possible sometimes are reported to retain a segmenta- origin of wings from a structurally "old" an- tion and musculature comparable to that of thropodan appendage on the upper part of the the legs (Matsuda, '76). In aquatic habitats, leg, is supported by two ancient and potential- the tracheopods are useful in locomotion, as ly significant links: the primitive wing was respiratory gills and as tactile organs. tracheated by a branch directly derived from It is highly probable that all Pterygota prim- the leg trachea and was moved by the leg itively had two sets of vestigial lateral abdom- muscles. inal appendages, the equivalent of wings (figs. 28, 47) and legs, occuring serially on all seg- Fin theory ments (fossil material supporting this point Bradley ('42) attempted to explain the old will be discussed in detail later). In modern enigma of why the pre-flight wings, while still pterygotes this ancient and serial dualism in too small to support an insect in the air, con- lateral appendages is fully preserved in the tinuously evolved characters necessary for meso- and metathorax, and is sometimes (future) flight, such as an increase in size, and clearly expressed in the prothorax, but is ob- the development of venation, flight muscula- scured or obliterated in the abdomen. It is well ture, and a complicated articulation. Accord- documented (Kukalova, '681, however, that ing to his hypothesis, ancient primarily ter- primitive fossil mayflies had nine pairs of restrial pterygotes became amphibiotic and wing-derived gill-plates. In the males of more and more adapted for excursions into the modern Ephemeroptera the leg-derived gono- water. However, they were probably capable styli are still present on the ninth segment. of leaving the water for purposes of mating Further evidence of serial dualism in the ab- and dispersal. Thus, the little pro-wings which domens of Paleozoic plecopteroid Protor- would have had little or no effect in air, could 70 JARMILA KUKALOVA-PECK have been highly useful as fins and propulsion gin of wings. As shown below, the amphibiotic organs in water. In the process of using pro- life in insects (or in other animal groups) is wings as fins, the hinge and flight muscula- not bound to cause distinctly aquatic struc- ture began to develop. An identical idea, in- tural adaptations. spired by the mechanical efficiency of pro- A proof that spiracles are not completely wings rowing in the water, was independently lost during aquatic adaptation in even Recent presented by Grant (’45). Ephemeroptera is provided by Durken (’07) At the time that Bradley (‘42) formulated and Landa (’48). In younger instars, all his “fin theory” of wing preadaptation, two spiracular tracheae (tracheae that are con- later contributions of fossil evidence were un- nected to the spiracles) collapse and are known: 1. That all primitive Paleozic nymphs marked only by a barely visible internal had articulated and movable winglets strand (figs. 37,401. An opened trachea is tem- throughout their ontogenetic development porarily formed before each molt and the (Sharov, ’57a,b, ’66, ’71a,b; Carpenter and lumen closes again after the old trachea has Richardson, ’68; Kukalova, ’68; Wootton, ’72; been removed with the exuvium. In the later Kukalova-Peck and Peck, ’76). 2. That the instars, however, the first and second thoracic Paleozoic aquatic mayfly nymphs probably spiracles do not vanish and their spiracular did use their articulated, lateroposteriorly ex- tracheae do not collapse. Instead, the spiracles tended wings like fins, as he anticipated for are only tightly mechanically closed (fig. 39). the early pterygotes (figs. 28,30). Consequent- Therefore, the thoracic spiracles of older ly, Bradley’s hypothesis, even if it erroneously ephemerid nymphs have persisted through explains the origin of the wing itself, seems to more than 250 million years of aquatic adap- somehow conform with the fossil evidence in tation. Similarly, in the nymphs of Odonata, the origin of flight. the abdominal spiracles are closed, but the Bradley’s (’42) and Grant’s (’45) view that thoracic spiracles do open and function in the the aquatic environment promoted a propel- final instar, before metamorphosis takes place ling function in small (nymphal) wings finds (Corbet, ’62). Hence, we should keep our minds support in the fossil record. It is quite evident open to the possibility that ancestral ptery- that use of the wings in some Paleozoic gotes were fully capable of switching their nymphs under aerial conditions was already environments and of thus exposing the wing decreasing. Thus, the wings in all terrestrial structures to varied functions and adapta- juvenile roaches were completely flightless. tions; it also should be noted that amphibiotic Some nymphal wings in Palaeodictyoptera, as life has led to the evolution of important judged by their general shape and position organs in many other groups of animals. (figs. 22,241, were in the process of rapidly los- ing their ability to function. At the same time, Gill-cover theory aquatic ephemerid nymphs used their wings The gill-cover theory by Woodworth (’06) to for promoting forward motion under water some extent bridges the previously discussed (figs. 28, 30). “spiracular flap theory” which associates the In opposition to the aquatic origin of wings, origin of wings with respiration, and the “fin H. H. Ross (’55) introduced the following theory,” which promotes the aquatic habitat facts: almost all living, generalized insects as the stimulator of pro-wing development. have normal functional spiracles in the imma- In the gill-cover theory, the origin of wings ture stages, and hence they were necessarily is assumed to have been conditioned by a also present in the juvenile ancestors. Aquatic change of habitat, when a formerly terrestrial juveniles became independently different insect became aquatic. In a small insect, of from their early ancestors (by loss of spiracles, about the size of a young mayfly or dragonfly etc.) and cannot represent an ancestral stage. nymph, the only necessary adjustment would In spite of the fact that Ross’ statement is be a reduction of the thickness and firmness of true (Paleozoic mayfly nymphs have long, cur- the cuticle, because cuticular respiration pro- sorial legs with no trace of any adaptation for vides a sufficient supply of oxygen. However, an aquatic environment; the obliteration of increase in size necessitates a substantially spiracles in Recent aquatic nymphs is dis- larger intake of oxygen as well as a hardening tinctly secondary, etc.), his reasoning is wrong of the body wall for muscle attachment. and cannot disprove the possible aquatic ori- Therefore, respiratory structures in larger in- INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD 71 sects become localized and improved by adap- the wings were continuously movable and the tations of the body wall. increase in their size between the first instar Gills, as the organs of aquatic respiration in and the adult was completely confluent (figs. insects, are in their simplest form any out- 6, 30, and unpublished material) and the growth of the body wall that retains the soft metamorphic instar was missing. Thus, be- texture originally possessed by the whole body cause of morphological reasons, there is a surface. The simplest outgrowth (blood gill) strong indication that the wings did originate becomes much more efficient if served by a in the nymphal stage and can be explained tracheal twig. Clusters of filamentous gills only through the possible function and tend to grow around the limb bases and other benefits that they brought to the juveniles, as protected but well ventilated areas. However, Woodworth fore-shadowed in his gill-cover a great many insects assist respiration by vi- theory. brating the body and by continuously bathing Synthesis of ideas on wing evolution the gills in water currents. When an insect possesses articulated covers protecting fila- In the preceding text, four theories on wing mentous gills, water circulation may be pro- origin are mentioned that are acceptable, at vided by movement of the covers. With such least partially or with some modification, in covers, older individual nymphs could have re- the light of the present fossil record. entered the terrestrial environment (if their Bocharova-Messner, (’71) in the “spiracular body cuticle hardened and their mechanically flap theory,” seems to have explained why the closed spiracles re-opened) and take advan- wing buds are always found near and above tage of these mobile, lateral appendages. the spiracles in view of the fact that the in- Thus, mobile gill-covers may have been sects were primitively terrestrial and had cur- preadapted for use as wings. sorial legs. Woodworth (’061,in the “gill-cover In his well documented study, Woodworth theory,” probably provides the most accepta- (’06)was inspired by the abdominal wings (he ble reason for the rapid evolution of the small called them gill-covers) of some mayflies, pro-wings, once some insects entered the which actually function as opercula for the water (through their generation of respiratory filamentous gill-clusters, protect them from currents), as well as for their placement above being clogged with silt in turbid water, and the spiracle. Bradley, (’42) in the “fin theory,” provide for them a circulation of water. He gives the most likely explanation for the per- noticed that these covers are stiffened by a fection and coordination of the base-rotation real venation, and the veins are even indicated musculature essential for flight in the larger by rows of spines as in flying wings, to which pro-wings. Wigglesworth, (’73) in the “stylus they bear a striking resemblance (fig. 25A). theory,” suggests why the wings are moved by However, he pointed out the difficulty in ex- the subcoxo-coxal musculature and why they plaining why, in ontogeny, there is the repres- give in many respects an impression of being sion of wing development until the final molt “old structures.” Further investigation is of the metamorphic instar (the essential pre- needed to support or reject any particular pos- requisite to the gill-cover theory is the sibility or any combination of them and the vigorous function of the gill-covers during the question is still open to hypotheses. whole juvenile phase). This “inconsistency” is I now take the opportunity of summarizing only seeming and is explainable on the basis of the above ideas and of offering a new recon- fossil evidence. struction of the origin of wings and flight. For The present fossil record complements more detailed discussion of the fossil record Woodworth’s data by revealing the venational and the origin of metamorphosis, the reader is pattern in the Paleozoic abdominal wings, referred to section IV of this paper. It is of which is much better preserved than in prime importance to remember that wings modern mayfly nymphs and is even compara- arose only once (as shown by the remarkable ble with that of the thoracic wings (fig. 28). degree of uniformity of wing characters) in The repression of the nymphal wings is shown arthropods, which are otherwise notorious for to be the derived condition which occurred the repeated and independent origin of very only after the wings were fully established as complicated structures. As emphasized by efficient flying organs in the adults (figs. 29, Woodworth (’06) and Wigglesworth (’631, this 30). In the primitive ontogenetic development event must have been exceptional and was fol- 72 JARMILA KUKALOVA-PECK lowed by extraordinary and potent selective haemocoel was restricted to channels, and the pressures favoring the growth of the pro- basic subcoxo-coxal musculature was devel- wings; otherwise wings would not remain, oped. Later, the channels became cuticu- among anthropods, unique to insects and/or larized and sclerotized, and changed into a would not have developed. stiffening venational framework. In this early Equally as important to this subject is to set stage of evolution the veins became slightly the scene by the reconstruction of the environ- rippled, and thus the pro-wings gained addi- ment in which the early insects lived. Mama- tional mechanical strength. Eventually the jev (’71) points out that the most ancient ter- pro-wings became large enough to be capable restrial plants - Psilophyta - (known first of promoting forward motion and diversified from the Upper Silurian) were moisture-lov- into the three larger thoracic and the smaller ing, growing only in the high humidity of abdominal pro-wings. At this stage, the rainy primeval “swamps.” This was the only ancestral pterygotes might have been amphi- available (but discontinuous) environment biotic, and therefore these first propelling at- with “terrestrial” vegetation, and the ap- tempts perhaps happened during underwater terygote insects probably originated and lived excursions. It should be noted that the in it. Very likely they inhabited moist niches ancestral pterygotes very probably had cur- and were “semiaquatic,” as they often still are sorial legs with five tarsal segments, short leg- today. They probably fed on decaying plant derived cerci (long cerci in silverfish, Palaeo- tissue, aquatic algae, and organic debris and dictyoptera and mayflies are secondary spe- some of them were possibly predators on small cializations) and a caudal filament longer organisms. By the Middle and Upper Devo- than the cerci. Therefore, auxiliary propulsion nian plant stature had increased and “forests” by fin-like pro-wings was much more impor- existed, with some small quantities of leaf tant in primitive forms than it would be in any fall. Under these circumstances, there was modern aquatic nymph. In adapting to under- probably a strong pressure on the presumably water rowing, the pro-wings had to become semiaquatic phytophagous insects to reach larger, and further cuticularized, and the the more leafy and tender parts of these taller wing-plane more deeply corrugated for addi- plants. In the patchy (and possibly temporary) tional strength. The rowing pro-wings also early forest habitats, the insects which came had to be equipped with mechanized venation, to possess flapping lateral appendages had a a rotating base, and coordinated musculature, distinct selective advantage in their ability to three features which are also essential for for- escape, to break a fall, and to disperse. In ward flight. When these insects took to climb- patchy habitats, dispersal through the utiliza- ing vegetation to feed, mate, and disperse, tion of air currents, soaring and flapping they had an ametabolous ontogenetic develop- flight might have carried a crucial survival ment like modern Apterygota. Their onto- value (Wigglesworth, ’76). genetic series included many nymphal and Wings are movable evaginations of the body subimaginal instars, so that no metamorphic wall above the spiracle and below the tergum. instar was necessary. The pro-wings were lat- In the early pterygotes, they were present on ero-horizontal and paleopterous. all body segments. The wings might have The forms which were equipped with the started as new structures, analogous to spurs, largest and best coordinated pro-wings had which were adapted as spiracular flaps or the better chance of survival, because the movable gill-covers, or they might represent old nymphs and adults could use them for old transformed structures. They could have breaking a fall, prolongation of aerial excur- first served as regulatory respiration mecha- sions, attitude control, etc. Finally, the wings nisms in a closing of the spiracles during tem- reached the size where they could be employed porary excursions into water and as an oper- in active flight, and the Paleoptera, as an culum preventing respiratory water loss after adaptive grade and taxon, became established. the insects took to the trees. Or they could The wings of the first Paleoptera were hinged have protected the gill tufts and bathed them to the body along a simple, straight line and in water currents, or served as lateral tactile could not be flexed backwards over the abdo- organs as, by analogy, do the coxal styli in men. Their ontogenetic development was still modern bristletails. confluent (ametabolous), but now became sub- In this first period of their existence, the jected to strong selective pressures: The sack-like pro-wings became flattened, the adults, in which the size of the wings was suf- INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD 73 ficient to keep them airborn, were pressed to genetic sense the ontogenetic development of further improve flight capabilities. The young Endopterygota does not differ from that of instars, which were unable to fly and had to Paleoptera and exopterygote Neoptera. escape through vegetation or by hiding, were Introduction to wing venation pressed in an opposite direction, to change the and corrugation impeding latero-horizontal position of the wings, and to develop additional aids to All integumental evaginations on the insect locomotion through specialization of struc- body, such as flaps, spurs, projections, or tures like legs, tails, body movements, and wings, are formed around an extended anal jets. haemocoel or blood cavity. If the evagination This “streamlining” evolutionary trend in becomes flattened, the remnants of the hae- the juveniles of most Paleoptera caused the mocoel are trapped between two layers of in- wings of early instars to grow in a curve with tegument and eventually become restricted to the tips directed backwards. This wing curve, channels which might protrude above the sur- also called the “nymphal wing bend,” in the face. These elevations of the epidermis and older instars became more and more straight- cuticle which conduct blood are usually not ened at each moulting, until the adult latero- corrugated and are generally called veins. By horizontal position was achieved (figs. 6a-f). this process, veins are produced in the telsonal In some other Paleoptera, the same trend plates of crustaceans, in the tails of damselfly caused changes in the alar articulation. nymphs, in the lateral expansions of galumnid Twice, at different times, a new group di- mites, or elsewhere in double-walled verged from the paleopterous stock, capable of arthropodan structures. It is believed here an active flexing of the wings backwards over that insect wings started as flattened the abdomen. In the first group, (fig. 46b), the evaginations and that the veins are derived third axillary sclerite was shifted into a pivot- from residual blood channels between the two ing position and all the hinge sclerites were basement membranes of the integument. rearranged into a V-shaped formation: this Such hypothetical, small flaps were not cor- led to the origin of Neoptera and triggered the rugated and perhaps adorned thoracic and ab- development of many peculiar new charac- dominal segments of Lower Devonian ters. In the second group (fig. 46a’) the actual ancestral pterygotes. The fossil record on this flexing mechanism was (somehow) different phase of evolution is lacking. from the “neopterous” type and the resulting The earliest winged insects on record (Pro- new order Diaphanopterodea stayed paleop- torthoptera, Paoliidae) were found at the terous in all remaining characters. The trend base of Upper Carboniferous in Poland and to suppress the nymphal wings continued in Czechoslovakia (Kukalova, ’58). In their both Neoptera and Paleoptera. The older in- wings, the venation occurred as cuticularized stars, with intermediately-sized wings, were tubes, the interspaces were formed by a dense neither good “flyers” nor good “hiders” and cuticularized archedictyon and thick mem- therefore were thus most exposed to selective brane, and the veins were corrugated into al- change. Eventually they were replaced by a ternating ribs like a fan for more mechanical metamorphic instar, which bridged the grow- support. These earliest-known wings differ ing morphological gap between the juveniles quite substantially from the hypothetical and adults while the wings of younger instars archetypal wing-flap. They were lighter, lost their articulation and were transformed stiffer, and much larger because of cuticu- into wing pads fused with the terga. In some larization, sclerotization, membranization, orders (i.e., blattoids), this process took place and allometric growth; they were articulated as early as in the Lower Carboniferous, in to the body by a sophisticated system of others (i.e., Ephemeroptera), later. Endop- pteralia and epipleurites; they were supported terygote Neoptera originated from early by tubular venation which formed a light but ametabolous exopterygote Neoptera (perhaps strong, mechanically efficient and intricately of a plecopteroid type) by reducing the wings, fluted framework; and the arrangement of legs, and many adult structures to mere this framework was definite and comparable imaginal discs which became invaginated un- to all known fossil and living winged insects. der the larval cuticle. The resulting larva was Hence, there is a big gap in the documentation very different from the adult and able to of how the venation evolved from a disar- invade extremely varied habitats. In a phylo- ranged, random pattern into a definite corru- 74 JARMILA KUKALOVA-PECK gated framework, homologous throughout the 9-11).The questions then are: (1) Why is the whole group of the Pterygota. paleopterous condition supposedly primitive For classification of wing venation, the Red- and the neopterous condition derived? (2) tenbacher System of nomenclature is em- How does the corrugation relate to the origin ployed in which six main veins are recognized of flight? Is it a contributing cause or a conse- (costa, subcosta, radius, media, cubitus, and quence of flight? And, (3) how important is it anal). Redtenbacher (1886) used the primitive for the function of modern wings? alternation of convex (+) and concave (-) Wing fluting in Paleozoic insects was gen- veins to homologize the venation of Pterygota. erally more common and pronounced than in Lameere ('23) noticed that there were origi- modern insects. There were six orders of nally two media veins (media anterior, MA; Paleoptera with a deeply corrugated venation, and media posterior, MP), and two cubitus only two of which have survived until Recent veins (cubitus anterior, CuA; and cubitus pos- times. In the extinct Paleoptera, the veins terior, CUP),one of each being convex and the were unreduced in number and the corruga- other concave. Carpenter, in many papers tion was deep and regular (fig. 7).In Paleozoic which he summarized in 1966, dealt with the and in living primitive Neoptera, the corruga- adaptive loss of convexities and concavities of tion is often more distinct than in the living some veins in most orders of insects. A con- specialized orthopteroid and plecopteroid tribution of the present account is that each of orders. Wing pads in living nymphs, as a rule, Redtenbacher's original six veins is recognized are almost flat with faintly indicated surface as being primitively composed of two veins, a ridges which do not represent true veins; how- convex and a concave one (fig. 45). I have ever, the Paleozoic nymphs had a tubular found the full pattern of six pairs of veins so wing venation which was functional as a sup- far in Paleozoic representatives of Palaeodic- porting framework and was fully corrugated tyoptera, Ephemeroptera, Odonata, Pro- (figs. 29, 30). Also the venation in the small todonata, Blattodea, Protorthoptera, and abdominal wings of Paleozoic Ephemeroptera Orthoptera; it is probably a general feature was corrugated (fig. 28). Corrugation was which was present in the ancestors of all present before the insect wing became lineages. The remnants of the full venation mechanized for forward flight (fig. 14) (an pattern are also preserved in innumerable liv- important point which will be discussed in ing insects, as discussed in section I11 of the more detail later). As observed by Adolf present paper. However, this primitive pat- (18791, Redtenbacher (18861, Lameere ('231, tern has been found fully corrugated only in summarized by Carpenter ('661, the convex or ancient Palaeodictyoptera (in all other in- concave position of the main veins is primi- sects, lA+ and 2A- tend to loose their corru- tively homologous in all pterygote groups and gation). evolved in the most primitive wings. In con- Corrugation occurs to some extent at least strast, the reduction of corrugation is gen- in the metathoracic wings of all insect orders erally secondary and evolved as later adapta- (figs. 5,7-12).The corrugation or fluting of the tions to specific conditions of aerodynamics, wing membrane is caused by the alternate OC- wing-flexing, etc. Thus, the Paleoptera repre- currence of convex veins appearing (in dorsal sent a more primitive condition than that of view) as cuticular ridges, and concave veins Neoptera (Carpenter, '76). appearing as cuticular grooves. When the dor- The flattening of venation in living Neop- sal and ventral surfaces of the wing of a tera generally occurs in both branches of the paleopterous insect, such as Ephemeroptera, media, in the sector radii, and sometimes in are separated by soaking them in 10%KOH, it the anterior cubitus. In thick tegmina or becomes evident that all convex veins are elytra almost all corrugation is lost and the always formed only in the dorsal membrane, veins become flat (neutral), or nearly so (figs. and all concave veins in the ventral membrane 10, 11, 26). In hemipteroid orders, the media (Spieth, '321, (fig. 5); and that the corrugation and the sector radii are fluted only weakly if is very pronounced. When Spieth's technique at all. In the orthopteroids s. l., the anterior is used on various neopterous insects, all veins branch of the media is mostly neutral and are impressed at least to some extent on both never distinctly convex; the posterior branch membranes as mirror images (Holdsworth, is either concave, or flat (fig. 261, (Carpenter, '41), and the corrugation is generally less pro- '66). In the endopterygote orders, the convex nounced in the central part of the wing (figs. anterior branch and concave posterior branch INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD 75 of the media have been retained (Carpenter, ancient Paleoptera (figs. 13,7,8),is secondary ’40, ’66; Adams, ’581, (fig. 9B). and highly adaptive and was derived from the The primary cause that started a chain of more primitive neopterous type of corruga- adaptations which finally led to the reduction tion, in which Rs and M were mildly flattened. of corrugation in Neoptera is believed here This is substantiated by, among other evi- to be wing-flexing. This major evolutionary dence, comparing the corrugation of higher event prompted the rearrangement of a flies with lower flies and that of their straight and primitive series of axillary ancestral order - the Mecoptera. In the opin- sclerites into a V-shaped series, so that the ion of Rees (’75) the mechanical properties of flexure could occur around the revolving third muscoid, hymenopteroid and other wings with axillary (see section 111). It also brought new deeply corrugated venation compare with requirements for the musculature and finally those of regularly folded or tubularly rein- for flight itself. All these changes were proba- forced beams. The varying depth of corruga- bly closely followed by the development of tion (figs. 8, 13) reflects the distribution of aerodynamic “passively deformable areas” aerodynamic forces: the stout bars which which, according to Wootton (‘76: XV. Int. sometimes occur near the wing base (fig. 7: Congr. of Entomology) are recognized by their abr; fig. 12: br) help to prevent fluted folds leveled corrugation, and occur most frequent- from opening out suddenly when under pres- ly in the vicinity of the veins Rs, M, and CuA. sure, the same manner as the crossbraces in a In some higher Neoptera, namely in special- corrugated roof of a building. ized Diptera and some Hymenoptera, the cor- Characteristic in the evolution of the wing rugation of the central wing area became sec- in all Pterygota is the early loss of corrugation ondarily deeply accented. In higher Diptera it in the anal area. Again, according to Wootton became even more intensified by the addition (’76, personal communication) the flattening of a supplemental highly convex “spurious is due to formation of aerodynamic “passively vein” which originated as a cuticular rib on deformable areas.” The secondary adaptation the back of the permanent wing-fold (fig. 13: of the anal area for better flight by a leveling sv). This secondary “revival” of corrugation of its corrugation happened so early that only was brought about by the change of flight some primitive Carboniferous and Permian technique, as explained by Pringle (’75): The Pterygota show a distinct fluting of the anal up stroke is accomplished in all insects veins, with 1A and its branches being all con- indirectly, by a depression of the tergum. The vex, and 2A and its branches being all concave down stroke in Paleoptera and primitive (fig. 71, (Kukalova-Peck and Peck, ’76). Usu- Neoptera is produced by direct (i.e., mainly ally both anal veins come to lie on an even to- subcoxo-coxal) muscles, attached to the base pographic plane in Paleoptera as well as in of the wing. The muscles attached to the Neoptera (figs. 9A,B). The leveling of the anal basalare twist the leading edge downwards, veins in primitive Palaeodictyoptera is dis- while the muscles attached to the subalare tinctly related to the formation of the “anal produce the reverse twisting movement. How- brace” (fig. 7A: ab), the crosswise cuticular ever, in most Neoptera, the down stroke re- bar that is also present in Recent Ephemerop- sults indirectly from an elevation of the tera (Kukalova-Peck, ’74) and which prevents tergum and higher wing speed in higher Dip- the anal area from buckling. tera and Hymenoptera is achieved by a special The corrugation of the principal veins de- click mechanism in the wing joint; twisting scribed above should not be confused with the (pronation and supination) of the wings oc- auxiliary corrugation formed by secondary in- curs automatically as the scutal cleft between tercalated veins, also called intercalary veins scutum and scutellum closes and opens and or sectors. These veins are formed from reticu- the wing rocks backward and forward over the lations and often multiply the fluting in a di- main pivot of the pleuron. It seems very proba- rection opposite to that of the main veins ble (though it is not yet fully explained on an (Martynov, ‘25; Sharov, ’66; Wootton, ’76). aerodynamic basis) that the latter changes in This type of secondary corrugation is most evi- flight technique described by Pringle (’75) are dent in the enlarged anal fans of the hind the main cause of the accentuated corrugation wings, especially of orthopteroid insects, and in higher Neoptera. randomly in other groups. The presence or ab- The intensity of fluting in higher Neoptera, sence of intercalated veins is rarely indicative although superficially similar to that of the of close phylogenetic relationships above the 76 JARMILA KUKALOVA-PECK generic or even the specific level. However, in from modern functional morphology, is not dragonflies and mayflies, they are apparently confirmed by the fossil record. On the con- exceptionally important and ancient apo- trary, indications are that fluting was already morphic features. present in pre-flight wings, before the One or two anterior branches of 1A immedi- mechanization of the venation had even ately proximal to CUP which are present in started. blattoid hind wings were called the “second A source of information on the possible mor- plical vein” by Forbes (‘431, (fig. 26). At the phology of pre-flight wings are the prothoracic same time, his “first plical vein” is, in phylo- winglets of Palaeodictyoptera (fig. 14).These genetic homology, the cubitus posterior (CUP), were primitively movable and articulated to and his “third plical vein” is the posterior the tergum (fig. 1). The venation of the branch of 1A. This kind of superimposed ter- winglets was fan-like in arrangement and was minology is confusing because it replaces ho- homologous to that of functional wings but mologous veins of the basic pterygote scheme the shape and the distribution of veins was not (CUP, 1A) by uniquely topographical terms. at all mechanically adapted for flight. Other confusing terminologies were in- How do we know that the palaeodictyop- troduced by Snodgrass (’35) and Wallace and teran prothoracic winglets were incapable Fox (’75) who called 1A of some Neoptera the of producing forward flight? Pringle (’75) “postcubitus”; by Smart (’51) who interpreted summarizes flight movements as follows: 1A in fore wings and the anterior branch of 1A “In order to produce the aerodynamic forces of in hind wings of roaches as a “postcubitus”; by lift and thrust, flapping wings have to move Hamilton (’71-’72)who designated the cubitus with the stroke plane inclined to the vertical, posterior (CUP) in pterygotes as the “plical and must make pronation and supination vein,” the first anal (1A) as the “empusal twists.. . .” In functional morphology it vein,” and the second anal (2A) as the “first means that the flying wing must have a anal vein”; and by others. Since the phyloge- stiffened anterior margin, that is, the vena- netic identities of CUP and 1A throughout tion must be rearranged by having C, Sc, and Pterygota are known (see paleontological lit- RI lined up along the anterior margin. The erature of the past 30 years; Brues et al., ’54; prothoracic winglets of early Palaeodictyop- Sharov, ’66; and “Insects of Australia,” ’701, it tera might have been capable of flapping up would be a regressive step to revert to a and down, but they could not actively fly or typological and topographical terminology. scull forward because they were not so Corrugation does not “jump” from the dor- adapted. The most interesting feature of these sal to the ventral membrane, as is sometimes leaf-shaped planes, however, is that they are erroneously presumed. The convex, concave, or already corrugated (fig. 14).This corrugation neutral position of the main veins is phyloge- is weak but distinct (personal observation in netically based and well established (Adolf, 1977) especially in dictyoneurid Palaeodic- 1879; Redtenbacher, 1886; Lameere, ’22-’23; tyoptera from Commentry, France (Kukalova, Spieth, ’32; and Carpenter, ‘40,’66). Changes ’69-’70).Thus, in these cases at least, corruga- occur slowly as a consequence of alteration in tion occurs not as a response to flight, but as a articulation and flight techniques. After an previous adaptation to another (yet unknown) entomologist is acquainted with the position kind of up-and-down movement which per- of flattened “passively deformable areas” in haps preceded flight. the more primitive (fossil and living) forms, Such pre-flight wings of ancestral ptery- he can use corrugation with confidence for gotes were apparently preadapted for flight in correct interpretation of venation patterns in at least four ways: 1. in the presence of true, all taxa of his particular group of interest. cuticularized, tubular veins; 2. in the corruga- tion which provided additional mechanical Origin of wing corrugation support; 3. in the presence of the reticulation In spite of the voluminous literature on between the veins which perhaps helped to wing corrugation, the timing of its appearance strengthen the wings as well as to conduct has been seldomly considered. The develop- blood; and, 4. in at least partial development ment of corrugation is generally presumed to of a hinge with sclerotized tergal sclerites and have been synchronized with the development basivenales. All these features are also found of flight, a seemingly well substantiated con- in the wings of primitive Paleozoic nymphs clusion. Nevertheless, this deduction, drawn (figs. 6a-c) which seems to give additional sup- INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD 77 port (through recapitulation) to this concept fossil evidence (fig. 45) that the primitive of pterygote pro-wings. The fact that wing- wing-base along the primitive straight hinge corrugation preceded flight strengthens the was not narrow, and that the veinal base of conclusion that paleoptery was ancestral to each corrugated vein was flat. The whole alar neoptery . part of the hinge was formed by the compact Judging from the morphology of the pro- series of flat basivenales, so that there was no thoracic wings in Palaeodictyoptera, the mechanical contact between the corrugated slightly protruding haemocoel channels in the vein-pairs and the tergal pteralia. Forbes pro-wings of early Pterygota were at first (’431, on the other hand, postulated that cor- spread fan-like and not fluted. They became rugation was a result of the articulation to the further cuticularized and sclerotized, proba- thorax, and the indirect action of muscles on a bly to reinforce the pro-wing by mass alone. few principal veins. Again, this explanation The excretion of cuticular material became does not conform with the fossil evidence. The uneven and differential, so that the profile of primitive hinge line (h) separates pteralia of the veinal tubes became asymmetrical when two morphological units, the thoracic and the excess cuticle was unevenly deposited on the alar (fig. 45). The flexible hinge is between the dorsal or ventral sides. The pro-wings then axillary sclerites, which are slanted mesad became rippled. The rippling was mechanical- towards the paranotal sulcus, and the fused ly advantageous and favored by selective pre- and flattened alar basivenales. These latter ssures. The pro-wings could become thinner completely separate the corrugated vein-pairs and larger without loosing strength. Because from the axillary sclerites. of the mechanical superiority of regular cor- Most entomologists agree with Edmunds rugation, the uneven deposition of cuticle and Traver (’54) that the thinning of the became stabilized in a regular pattern; the wing-membrane, and the origin of fluting in blood channels which were incipient veins the wings were simultaneous. To be capable of grouped together into six paired systems, each sculling flight the main wing blade had, first, one connected with the body haemocoel by a to be thin and flexible. Secondly, it needed a single basal blood sinus. The anterior branch firmer support than the veins themselves of each paired system became convex because could provide. The necessary rigidity was of excess deposition on the dorsal side and the secured by fluting. The relationship between posterior branch concave through deposition thinning and fluting is well demonstrated in on the ventral side. The process finally re- cross sections of various corrugated wings sulted in alternating ribs regularly protruding (figs. 7-9, 12): in thin membranous wings the in opposite directions. The amazing regularity corrugation is amplified by asymmetrical and symmetry in the vein-pairs, in their thickening of the dorsal part of convex veinal branching and corrugation, seems to correlate tubes, and of the ventral part of concave with the symmetrical leaf-like shape of the veinal tubes. In contrast, the corrugation be- palaeodictyopteran pro-wing, as well as with comes secondarily diminished if the cuticular the even fan-like distribution of the primitive veinal tubes are thickened symmetrically, as veinal framework. All these features strongly in tegmina and elytra, in both dorsal and ven- suggest that the pro-wings were engaged in tral parts (figs. 10, 11). some function which required up and down According to Wootton (’76: XV. Int. Congr. movement (as spiracular flaps or gill covers). of Entomology), “Insect wings, which are con- The ripples, inconspicuous at first in the ventionally illustrated as flat planes, are real- pro-wings, became crucially important after ly intricate 3-dimensional structures whose the juvenile winglets became involved in primary function is the translation of small motion. In this process, the wings increased in axillary movements into complex flight pat- size, the corrugation deepened, and the vena- terns.” In the pattern of the wing venation, he tion became mechanized. Finally a stage of de- recognized “passively deformable areas,” velopment was reached whereby the corru- usually marked by diminished corrugation gated wings could produce active forward and “supporting/deformation areas,” which flight. are corrugated or otherwise reinforced. The The origin of fluting was attributed by relative position of these areas determines the Needham (’35) to the gathering together of angle of attack and the generation of useful the basal connections of the veins, and the aerodynamic forces. According to this expla- narrowing of the base. We now know from the nation, an increase or a reduction in corruga- 78 JARMILA KUKALOVA-PECK tion follows closely after changes in the axil- shorter legs. The fossil record shows that laries and other features of the wing that wings of the oldest known insects (found at adapt to aerodynamic forces. Thus, the primi- the base of Upper Carboniferous) are distinct- tive flattened central part of the wing vena- ly larger than those of the average modern in- tion in Neoptera can be explained as a new sect; the legs are not noticeably shorter, ex- "passively deformable area" and is an adap- cept in some flying forms with large wings, tive response to the changed arrangement of such as some Palaeodictyoptera. axillary sclerites. Special attention should be given to the What is not known is the reason why the resting position of the primitive wings. Early pre-flight thoracic pro-wings became larger, pterygotes, as summarized in this paper, were thinner, and stiffened by a corrugated vena- paleopterous. Hence, the first terrestrial tion, and thus became preadapted for flight. adults had their wings spread out laterally, There is no conclusive fossil material to indi- not postero-laterally as they are generally re- cate whether this process happened in the constructed. According to Neville ('65), the aerial environment, in the aquatic environ- wings of modern soaring dragonflies are in ment, or in a combination of both, and we are elastic equilibrium and therefore are held in a confined to mere hypothesis. However, the horizontal position without effort. It is proba- fossil record may, in the future, present more ble that this energy-saving type of flight was "down to earth" evidence. also present in early Paleoptera. Apparently the first flying Pterygota were able to soar ef- Flight efficiency fortlessly on their outspread wings and to The musculature used for primitive flap- switch to flapping flight at will in order to ping flight was the subcoxo-coxal muscles, choose a landing site or to prolong flight (fig. which were already present in the aptery- 46B). gotes. Therefore, the pro-wings were almost A comparative study of neuromuscular certainly movable long before the articular mechanisms shows that the wing beat in early structures were fully differentiated and be- flying pterygotes would have been much fore the pro-wings enlarged in size. This suc- slower than in the majority of today's insects cession is still reflected in development of (Ewer, '63). Since thrust is related to the fre- the abdominal winglets of modern mayfly quency of the wing beat, the resulting speed of nymphs (Durken, '23). As suggested by Ewer flight was also bound to be low in these primi- ('63) and Ewer and Nayler ('671, the primitive tive and unspecialized forms. For aerody- coordinating mechanism of flight movements namic considerations, slowly beating wings might have stemmed from that used in run- require a larger surface to obtain lift; the in- ning movements, and both running and flying duced drag (caused by trailing and tip vor- could have been served by a common central tices) could have been substantially reduced nervous pattern of control; since flapping by a lengthening of the wings (Neville, '65). flight involves a well coordinated, complex The fossil record shows that in the Paleozoic program of muscular movements, it could not the ratio between the size of the wings and the have arisen by some macro-mutation, as is body was conspicuously different than in sometimes proposed, but solely through gradu- modern insects and that the wings were rela- al selection. tively larger and longer (see Handlirsch, '06, Most likely, the first excursions of insects for data on size). I assume that a combination through the air were by dropping to avoid of all the above mentioned aerodynamic fac- predators or by being involutarily blown from tors caused the well known gigantism of a high object by the wind (Zalessky, '53; Ewer, Paleozoic insects, with their relatively over- '63; Wigglesworth, '63; Hinton, '63; Flower, sized, long and broad wings. '64). In a study of the aerodynamic behavior Opposite selective pressures towards small- of insects of different shapes, Flower ('64) er insects with more manoeuverable wings showed that in larger insects the presence of and greater concealment ability occured later even rather small pro-wings would favorably and has been pronounced since the Upper Per- affect attitude, provide greater manoeuver- mian. I suppose that a prerequisite for this ability during descent, and considerably in- tendency was the ability of a particular group crease the distance that could be covered lat- to increase the frequency of the wing beat. A erally. Selective pressures would then favor faster wing beat resulted from better coor- larger and more manoeuverable pro-wings and dination of the musculature, acceleration of INSECT WINGS. METAMORPHOSIS. AND THE FOSSIL RECORD 79 respiratory and muscular metabolism, im- towards the end of an ontogenetic line does it provement of muscle relaxation and neuro- come to closely resemble the adult venation. muscular mechanisms, and “automatization” Finally, the epidermal cells lining the lacunae of structures participating in flight. This ulti- secrete the cuticle which form the walls of the mate evolutionary achievement helped to tubular veins. Only shortly before the turn insect flight into the energetically most emergence of the adult do the veins become efficient muscular activity known. This was formed and corrugated, and the epidermis de- reached by storing elastic energy in cuticle, generates. By then, the adult wing membrane muscles, and rubbery ligaments of the wing and veins are almost completely composed of hinge and releasing it again in automatically cuticle. functioning and repetitive cycles (Neville, Consequently, modern nymphs have uncor- ’65). rugated blood lacunae and the cuticular, cor- rugated venation is formed around them only 11. Origin and development of the alar in the final nymphal/adult moult. The “vena- circulatory system tion pattern” indicated on the wing pads of Blood circulates continuously in the wing modern nymphs (fig. 29) are cuticular ridges pads of nymphs and in the membranous wings which are not connected with the blood (as well as in sclerotized elytra or tegmina) lacunae (compare figs. 3 and 4). However, they of adults. Circulation transmits nutrients, are rudiments of what once was the nymphal water, and mechanical pressure, and plays a venation. Its repression and the postponement role in metabolism and perhaps also in res- of the development of tubular veins above and piration. It is necessary for physiological under blood channels until the very end of the equilibrium, the normal development of nymphal stage mostly occurred after the sclerotization and pigmentation, and for the Paleozoic. It was independently acquired in overall healthy condition of the wing in all all the then existing evolutionary lineages stages of adult life. A cessation of circulation leading to modern insects. This fact has soon makes the wings brittle and results in a important implications for the interpretation cracking away of “dry” parts (Arnold, ’64). of metamorphosis, as will be discussed in more According to Arnold (‘64) blood is brought to detail later. the wings through alar blood sinuses via veins, According to Tower (’03) and Bodenstein cross venation, and reticulation (figs. 42-44). (’501, in the ontogenesis of modern Endop- It is continuously leaking from some of the terygota the slowly growing wing evagina- veins and to some extent probably percolates tions underneath the larval cuticle have no or diffuses between the basement membranes distinct traces of future veins. In the prepupal (fig. 41). instar the haemolymph is forced through the foramen of the wing and opens up visible Circulatory system in modern and primitive lacunae (remnants of the wing cavity, vein wings of juveniles anlage) between the two basement mem- Veins are cuticularized, tubular continua- branes. In the pupal instar these lacunae be- tions of the body haemocoel. They conduct come more marked and their width is reduced. blood, nerve fibres, and tracheae and give sup- Before the emergence of the adult they be- port to the wing. In the ontogenesis of modern come tubular. In newly emerged imagos the Paleoptera and exopterygote Neoptera, the wings straighten through pressure of the fluid veins develop from free blood spaces, the between the two epidermal layers and only lacunae, between the basement membranes after that do the wing veins harden. (fig. 4: Cu +A, R + M, Sc, C). Lacunae, as far as In Paleozoic insects, the ontogenetic de- is known, are not corrugated (Holdworth, ’41; velopment of the circulatory system was quite Woodring, ’621, (figs. 3, 4). They are at first different. The lacunae were already changed formed by epidermal cells only in the dorsal into cuticularized tubular veins in young integument (fig. 4, Cu+A, DE). After being nymphs (figs. 2, 6a-c, 22, 28, 30, 31, 35). Even “shifted’ into the wing pad, the lacunae are the smallest nymphal wings were movable completed by the application of the epidermis and articulated and were in need of being sup- of the ventral integument (fig. 4: VE) and ported by the venation (Kukalova-Peck and they thus gain a mirror-symmetrical tubular Peck, ’76). Therefore, the sclerotized and profile (fig. 4: R + M, Sc, C). The pattern of the cuticularized veins primitively are not solely lacunae changes in each instar and only adult structures. 80 JARMILA KUKALOVA-PECK

Evolutionary changes in blood flow accessible to the blood stream entering the wings from the body. Because blood could not In modern insects, the blood generally flows circulate through the primitive wing, it in all from the thoracic perivisceral sinus into the probability pulsed in and out through parallel anterior sinus, an area below the axillaries veins. The blood entered the wing through six which is merely an extension of the haemocoel wide blood sinuses (C, Sc, R, M, Cu, A of figs. (fig. 41) (see Chapman, '69, for references). 45A,B), and exited through the same basi- From there, the haemolymph usually enters venal openings. the remigial wing circulation through the sep- In search for a possible retention of this arate or fused blood sinuses of the respective primitive circulation in modern insects, I veins. These sinuses at the veinal bases are found that blood flow, according to Arnold sclerotized and form basivenal sclerites (also ('641, is generally somewhat variable in all in- called alar pteralia) which are designated by sect orders. Smaller accessory loops and local the names of the veins: basicostale, basisub- individual variations in circulation are quite costale, basiradiale, basimediale, basicubitale, frequent and the entire direction of flow can and basianale (figs. 45A,B: C, Sc, R, M, Cu, A). be reversed for periods of time. Likewise, indi- The blood enters the wing usually only vidual veins, like M and Cu in Orthoptera and through the anteriorly located sinuses and some other orders, can have a 2-way flow flows distally to the wing apex through the rather than a flow in predominantly one di- large anterior veins, C, Sc, R, and in some rection. In mayflies, the general loop-like cases M and Cu, and moves through cross blood flow, which is similar to that in all other veins towards the posterior margin. From modern orders, often alternates with an inter- there it returns through the posterior part of mittent refluxing of blood into and out of the the circumambient C, usually via Cu and A wing. This exceptional phenomenon has been into the body, by way of the axillary cord (fig. attributed to the broad basal sinus and the 44). After passing the cord (figs. 42, 43), the pliable nature of the body wall, or to ineffi- blood empties into the pericardial sinus or into cient pulsatile organs (Arnold, '64). However, the dorsal vessel. with the new data now available in the fossil The physical prerequisite for the steady record, a more probable explanation of this loop-like transport of haemolymph is the so- particular refluxing seems to be a plesio- called circulatory gradient. While the clus- morphic reflection of the primitive type of cir- tered axillary sclerites hold the membranes culation through the serial veinal systems. partially open to the flow of blood into the an- The blood sinuses at the base of the wings terior veins, access into the posterior veins is are as responsible for the origin of flight as are closed by a sealing of the posterior articular the veins. When sclerotized, they form the membrane (fig. 41: black area). The only exit alar part of the primary hinge. Another blood for a blood stream leaving the wing is the axil- sinus which occasionally participates in flight lary cord. These adaptations create the gra- mechanics is the pterostigma (pigmented spot dient and force the blood to flow around in a at the distal anterior wing margin). The role single loop (Arnold, '64). of the pterostigma is probably mostly physio- In the wings of primitive pterygotes (fig. 45) logical (Arnold. '63). However, in the dragon- this modern sort of circumambient blood cir- fly wing, the pitching moment of the cuit was not possible for the following reasons: pterostigma prevents torsional deformation of the costa did not encircle the wing but ended the corrugated surface during flight accelera- at the apex (and could not provide a posterior tion (Rees, '75). passage); the axillary cord, which is the main The blood stream is kept in motion by dif- exit for the efferent blood stream in modern ferent means, but mainly by aspiration insects, was not developed; the basivenales through thoracic pulsating organs (see Chap- (blood sinuses) were all widely opened, serial, man, '69, for references). They consist of a and extended across the whole wing base (fig. muscular plate which encloses a blood space 45A: C, Sc, R, M, Cu, A); and the axillary beneath the dorsal wall of the thorax, often in sclerites and tegula were also serially the scutellum; in some insects the dorsal ves- arranged, and provided uniform access to the sel may itself loop up to the dorsal surface to flow of haemolymph (fig. 45A: t, 1, 2, m). Con- aspirate blood, in which case the muscular sequently, a circulatory gradient never oc- plate is beneath the scutum. Special pulsatile curred and all veins were equally opened and membranes also occur in the veins of some in- INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD 81 sects and either conduct the blood centripetal- metathorax and subcoxa, University of Illi- ly or centrifugally. It seems possible that the nois in Urbana). Both specimens are probably scutellar pulsatile organ was present in the related on the generic level and were found in highly domed scutellum (sct in fig. 45A) of the Upper Carboniferous deposits (Westpha- primitive homoiopterid Palaeodictyoptera. lian C-D) near Mazon Creek, Illinois, by Mr. Some other accessory thoracic pulsatile and Mrs. Wolffe and Mr. J. C. Carr. Preserva- organs and/or veinal pulsatile membranes tion of the pteralia is good because of the large were almost certainly engaged in supplying size of the specimens. The set of pteralia is not blood to the six pairs of veins in the primitive complete in either specimen but each is com- wing circulatory system. plementary with the other, so that the full series can be reconstructed between the two of 111. Origin of wing articulation them without additional hypothesizing. In The origin of alar pteralia has not until now figure 45, based mainly on specimen No. PE been understood. Entomologists have made 16138, the second axillary sclerite, prealare, several assumptions: that at least some axil- suralare and tegula, have been reconstructed laries are actually extended veinal bases after specimen No. 2 (Carr coll.). The diagram (Matsuda, ’70; and for references: Hamilton, of the thorax and adjacent wing base (fig. ’71-72);that the tegula is not serially homol- 45B) is a generalization of specimen No. PE ogous with the axillaries; that the detached 16138 and an attempt to homologize pteralia third axillary, responsible for wing flexing in of modern Paleoptera and Neoptera with a Neoptera, has its detached equivalent in simplified, primitive, paleopterous pattern. A Paleoptera; that the proximal median plate in detailed comparative study of the articular re- Neoptera is of uncertain origin and does not gion in Paleozoic and Recent Odonata and occur in the Paleoptera; and that the so-called Ephemeroptera, and a comparison between “axillary plate” at the base of the wings of both orders, is currently in progress. Prelimi- Ephemeroptera and Odonata cannot be com- nary results helped to identify homologous pared with any structure in the Neoptera. A pteralia but, because of the quantity of docu- unifying concept on the origin and homol- mentary material, they have to be published ogization of pteralia has never before been separately. The taxonomic and morphological offered. study of the homoiopterid thorax, wing, and A phylogenetic evaluation of ancestral pleuron will be treated in a separate article. pteralia suggests an obvious way for unravel- ing the riddle. Since Neoptera are believed to Interpretation of pteralia in primitive have evolved from Paleoptera through the Palaeodictyoptera acquisition of a flexing mechanism in the In the articulary region of Palaeodictyop- wing articulation (Carpenter, ”i’l),the ar- tera (Homoiopteridae) (figs. 45A,B), the hinge rangement of very primitive pteralia in fossil line (h, wavy lines in fig. 45A) separates the Paleoptera might well provide the needed tergal unit composed of tergal pteralia includ- clues. Since modern paleopteran and neop- ing tegula and axillary sclerites (t, 1, 2, n-m, teran pteralia are difficult to compare, they 3) from the alar unit composed of alar pteralia would possibly be more easily comparable including basivenales (C, Sc, R, M, Cu, A). with what is close to the common ancestral Consequently, the primitive paleopterous form. hinge is a composite structure in which both With this in mind, I have searched the units participate. In the formation of the available fossils of primitive Paleoptera (Pa- tergal articular structures, the tergum proba- laeodictyoptera, Megasecoptera, Diaphanop- bly became incised by fissures and was then terodea) since 1960 for suitable sets of divided into five lobes posterior to the prealar pteralia, but found them either incompletely arm (PRA): the prealare (p),the suralare (s), preserved or too specialized. Then, in 1975, the median lobe (me), the postmedian lobe through the courtesy of Doctor E. S. (pm), and the posterior notal wing process Richardson, Jr. (Field Museum, Chicago), I re- (PNP). The lobes became slanted distally into ceived two thoraxes of gigantic Palaeodictyop- the deep sulcus, here called the paranotal tera from the very primitive family Homoiop- sulcus (pa, striped lines in fig. 45A). A series teridae (specimen No. PE 16138, metathorax of tergal sclerites separated from the tips of and hind wing, Field Museum of Nat. Hist. in the lobes and became slanted upwards, form- Chicago; and specimen No. 2, coll. J. C. Carr, ing their side of the convex hinge line: the 82 JARMILA KUKALOVA-PECK tegula (t)separated from the prealare (p); the costal branch or cross vein) and subcosta pos- first axillary sclerite (1)from the suralare (s); terior (Sc-1; radius anterior (RI+) and the second axillary sclerite (2) from the radius posterior (Rs - , sector radii) ; media an- median lobe (me); the median sclerite (m) terior (MA+) and media posterior (MP -); with the small detached notal median sclerite cubitus anterior (CuA +) and cubitus poste- (n) from the posterior median lobe (pm); the rior (CUP -1; anal anterior (AA, known as third axillary sclerite (3) and sometimes the 1A + , first anal vein) and anal posterior (AP, fourth axillary sclerite (4) from the posterior known as 2A -, second anal vein). notal wing process (PNP). In this way, a regu- The venation presented schematically in lar series of tergal sclerites originated, in figure 45 is actually the most primitive known pterygotes, by their detachment from five lat- condition (preserved in specimen No. PE eral tergal lobes. The sclerites were probably 16138 and some other Palaeodictyoptera). primitively manoeuverable by tergo-pleural Paleozoic Ephemeroptera, Odonata, Pro- (axillary) muscles. Most of these muscles todonata, Protorthoptera, Orthoptera and probably became reduced, with the exception Blattodea have well preserved posterior costa of those to the second and third axillary, and (C -) and anterior subcosta (Sc +) (personal some muscles of the lobes (mainly the prealare observation, to be discussed in a later and PNP). The wing flexor in Neoptera is at- account). tached to the third axillary. In Recent Paleop- Later, this complete venation pattern un- tera, the third axillary is an inconspicuous derwent many modifications, especially in the sclerite at the end of PNP. anterior and posterior part of the wing. How- The five tergal lobes on the tergal side of the ever, except for the obsolete costa posterior hinge meet the six sclerotized veinal bases (which became fused with the costa anterior (basivenales, blood sinuses) on the alar side of to give more support to the anterior margin), the hinge. The hinge itself is homologous to all other veins are present in more generalized the part of the dorsum separating the tergum modern Paleoptera, as well as Neoptera, and and the wing evagination early in ontogeny. can be phylogenetically identified and homol- The hinge-line was primitively straight and ogized. A detailed account of the complete mesally paralleled by the deep paranotal scheme of wing venation and its application to sulcus (pa). Primitive tergal sclerites are the venation of modern pterygote orders will arranged in a straight and regular row. Primi- be presented in a later paper. A likely explana- tive basivenales follow the pattern and also tion for the origin of the unpaired mid-dorsal form a straight row with the exception of the apodemal pits of the modern odonatan thorax basicostale (C), which protrudes slightly prox- is suggested in the migration of apodemal pits imally. (ap in fig. 45A), which in Palaeodictyoptera Basivenales are cuticularized and sclero- are located mesally to each median lobe. In the tized blood sinuses, through which blood circu- ancestors of the Odonata, the apodemal pits of lated back and forth in the primitive wing (see the two sides of the body migrated mesally and section on evolution of blood circulation). anteriorly and finally became fused into a From each basivenale two branches arise single, apodemal pit in mid-dorsal position. which in pre-flight wings were very probably The second axillary, which presumably fully independent: the convex anterior detached from the median lobe, articulates branch, and the concave posterior branch. with the first axillary and median sclerite in Early in their evolution, the pairs of the Ephemeroptera and Neoptera; in Odonata, it branches of R, M, and Cu became fused into became fused with the first axillary and with common basal stems, a condition which is the basivenal plate (Neville, '60).The postme- probably primitive for flying wings. The full dian lobe (pm) is rudimentary in modern in- primitive venation pattern of Pterygota (fig. sects but its respective detached sclerite, the 45) consists of the following veins: costa ante- median sclerite, is well represented in Paleop- rior (C + ), and costa posterior (C -, discernible tera as well as in Neoptera; in Ephemeroptera, as a separate vein only in most ancient fossil it was misinterpreted as the third axillary insects); subcoxa anterior (Sc +, costal brace (Matsuda, '56, '70; Tsui and Peters, '72); in of Ephemeroptera, humeral vein of some Odonata it was erroneously defined as the Neoptera if rising from basisubcostale) ; the third axillary by Hamilton ('71-'72); the small humeral vein of other Neoptera starts directly notal median sclerite (n), apparently sepa- from Sc and is an aerodynamically based sub- rated from the proximal part of the median INSECT WINGS, METAMORPHOSIS. AND THE FOSSIL RECORD 83 sclerite (m), has been detected in the with the basimediale, and the basimediale fre- Palaeodictyoptera. In Neoptera, the median quently fuses with the basicubitale (to form sclerite is identical with the so-called “prox- the so-called “distal median plate”). The ante- imal median plate” of Snodgrass (’351, which rior portion of the basianale, at which 1Ai was misinterpreted as a flange of the third ax- starts, has the tendency to become detached illary (Snodgrass, ’52; Hamilton, ’71-’72).The and migrate towards the basicubitale, with so-called “distal median plate” of Snodgrass which it might eventually fuse. This phenom- (’35) is composed of alar veinal bases and cor- enon is aerodynamically based and associated responds usually to the basimediocubitale. with the formation of the claval furrow in the The posterior notal wing process (PNP) is clavus, which is one of the principal support- present in both Paleoptera and Neoptera, and ing, deformation-limiting areas of insect the third axillary sclerite is formed from its wings (Wootton, ’76: Int. Congr. of Entomol- tip (as indicated in Recent Paleoptera). In ogy). This migration somewhat obscures the Paleoptera, the third axillary is usually sepa- identity of lA, so that it was given other rated from the PNP by a suture and is only names by some authors (postcubitus by Snod- slightly detached at most; in Neoptera, it is grass, ’35; Wallace and Fox, ’75); third plical distinctly detached and rotated, so that it can vein by Forbes, ’43; empusal vein by pivot about its point of articulation with the Hamilton, ’71-’72).Phylogenetically, this vein PNP and pull the wings into the flexed posi- is the first anal (lA),the convex branch of the tion. This ability of the third axillary sclerite, primitive anal veinal pair. The second anal together with the consequent V-shaped (2A) was primitively concave and, in Recent arrangement of all tergal sclerites and with insects, it became more or less flattened and the basal fold running through the hinge-line, forms the anal fan. Both anal branches 1A and are the principle apomorphic (key) characters 2A are homologous in all winged insects. In of Neoptera. In Hymenoptera and Orthoptera the phylogenetic sense, there is no 3A, 4A, etc. there is a fourth axillary sclerite, also which authors have frequently described, detached from the PNP. because these are merely the (detached) The alar side of the hinge is formed by branches of 2A. sclerotized basivenales (veinal bases). In Re- In ancient Palaeodictyoptera, the thoracic cent Paleoptera, the basivenales posterior to tergal lateral lobes are better indicated than the basicostale (humeral plate) increased in in any modern insects (fig. 45A). The sequence size and fused together into a large basivenal of the tergal axillary sclerites, and their plate (axillary plate of Snodgrass, ’35). The detachment from the respective lobes, is quite basicostale (humeral plate, humeral complex) clearly shown by their position. Their identity in both Paleozoic Odonata and Ephemeroptera is obvious, because their arrangement is sim- (unpublished material) is much enlarged; ple and serial; therefore, they can be fairly according to Neville (’60)the musculature easily homologized with the pteralia of vital for an odonatoid type of flight is attached modern Paleoptera and Neoptera. In the alar to the enlarged basicostale. In Recent part of the hinge, the basivenales are widely Ephemeroptera, however, the basicostale has opened towards the body cavity and arranged degenerated to an inconspicuous plate. The so that they extend across the entire wing- basivenal plate in Odonata is formed by all base. This position is very suggestive of their basivenales posterior to the basicostale and by role in primitive blood circulation and articu- the first and second axillary sclerite, all fused lation, as previously mentioned. All these together into one plate. In Ephemeroptera, the facts are extremely helpful in understanding basivenal plate is formed only by a basisub- the pterygote articular region and in provid- costale, basiradiale and basimediale, and is ing evidence for its monophyletic origin. followed by the large, triangular basicubitale My search in Paleozoic fossil material for (misinterpreted as third axillary sclerite by ventrally located sclerites (epipleurites), the Brodskii, ’74) and by a small basianale basalare and the subalare, to which the direct (Kukalova-Peck, ’74b). flight muscles (subcoxo-coxal muscles, etc.) In Neoptera, the basivenales are never large attach and which are therefore the most and do not fuse to such an extent. The important for the origin of flight, has so far basicostale (humeral plate) is inconspicuous, been fruitless. Specialists generally agree the basisubcostale rarely fuses with the that the basalare and subalare became basiradiale, the basiradiale sometimes fuses detached from the dorsal part of the subcoxa 84 JARMILA KUKALOVA-PECK

(pleuron) immediately under the base of the backwards? (2) Why are the wings of all wing. The subcoxa, pleural suture, kata- modern nymphs, both paleopteran and neop- pleuran ring, anapleuran ring and trochantin teran, oriented obliquely backwards, and how are, to my knowledge, all preserved in only one does this relate to the primitive pterygote specimen of a primitive Paleozoic paleopteran wing position? (in Palaeodictyoptera, Homoiopteridae, from Before discussing these questions with the Mazon Creek, Illinois) and this will be de- help of fossil evidence, it would be useful to scribed in another publication. point out some mechanical laws which, in The above concept of the tergal origin of all Paleozoic pterygote nymphs, have affected axillary sclerites and the tegula finds support the movement of wings of different sizes, in the ontogenetic studies of Neoptera- while they were still functional nymphal Polyneoptera by Bocharova-Messner (’68). In structures. her paper it was shown that the musculature In an aerial environment, a small wing is re- associated with the axillary sclerites is, by strained by aerodynamic laws and unfitted for its origin, definitely tergo-pleural. The pri- active flight. In an aquatic environment, a mary role of tergo-pleural muscles was to small wing may prove to be comparatively strengthen and support the shape of the seg- much more useful for propelling the animal ments before the skeleton became sufficiently forward. But, other things like legs, tails, body sclerotized. The pleuro-sternal musculature, movement, or anal water jets, can serve as namely basalar and subalar muscles, had the more powerful swimming tools, as demon- same primary destination. In modern weakly strated in modern aquatic beetles, waterbugs, sclerotized Polyneoptera, such as roaches, mayflies and dragonflies. Therefore, in both these muscles are still bifunctional and at environments, small wings were comparative- least partly continue to support the skeleton. ly inefficient devices for forward movement. In more tagmatized Polyneoptera with firmer If the small wings extended laterally, they skeleton, such as grasshoppers, this muscula- would impede the nymph’s forward movement ture assumes mostly the role of alar locomo- among vegetation on dry land as well as in tory organs. Thus, the ontogenetic study water. It is thus a matter of survival for both shows that the axillary sclerites and tegula terrestrial and aquatic nymphs to keep their are primarily supported by a tergo-pleural set small wings from hindering their motion. of muscles, while the basalar and the subalar On the other hand, as soon as they were sclerites, which presumably separated from large enough to serve in flight, wings were ex- the subcoxa, are served by pleuro-sternal mus- tremely useful for dispersal, migration, mat- cles. This finding is in accord with the origin ing and escape, and their value for survival in- of pteralia as it is indicated by fossil record. creased in linear relationship to maturity, reaching a peak in the adults. The resulting IV. Wings and metamorphosis evolutionary trend would therefore be 2-fold: Primitive position of wings in nymphs to keep small wings out of the way by stream- As explained by Bradley (’42) and others, lining young nymphs, and to deliver wings in only the meso- and metathoracic wings are in full size and undamaged condition to the adult a mechanically suitable position to function in stage, where they are most useful. flight. Hence, the prothoracic wings of the In the course of evolution, this adaptive primitive complete series gradually became problem was solved in two sequential phases. reduced or engaged in other functions (leg- During the first phase, which is well docu- and head protection), and abdominal wings mented in the fossil record, the wings of the vanished with the exception of those in mayfly nymphs remained articulated and movable nymphs, in which they still aid in locomotion. but became streamlined (fig. 46:a, a’, b). In The discussion in the following text is con- the paleopterous orders of the Pterygota (fig. cerned with the meso- and metathoracic wings 46:a, a’) this task was accomplished either by that are referred to only as “wings.” development of the so-called “nymphal wing There is at present no agreement on the bend” (the curvature in the basal third of the question of the primitive position of the wings wing which turned the tips obliquely back- in the pterygotes. The disputed points are: (1) wards as in fig. 46:a), or by flexing the wings Which condition was more primitive: wings backwards over the abdomen (in the extinct oriented laterally or wings oriented obliquely- order Diaphanopterodea) by a different mech- INSECT WINGS. METAMORPHOSIS. AND THE FOSSIL RECORD 85 anism than in Neoptera (fig. 46:a’). In the had not yet developed an expanded anal fan in earliest Neoptera (fig. 46:b) the same problem the hind wing, which had richly branched of streamlining was solved by flexing the venation, and whose macrotrichia were scat- wings backwards with the help of the pivoting tered on the wing membrane. From the availa- third axillary sclerite. This evolutionary ble fossil record, I consider members of the advancement eventually became the key family Strephocladidae (their “endoptery- character of the Neoptera. It is believed here gote” features have been pointed out by Car- that the wing-flexure occurred first in the im- penter, ’66) to be rather close to these matures, but it proved to be very advan- hypothetical ancestors. tageous for the adults as well. Thus, the evolu- As discussed and documented in more detail tion of wing flexing is viewed as having by Sharov (’57a, ’66) the ancestral stock of started as an adaptation for better streamlin- plecopteroid Protorthoptera, as far as is ing in the juveniles. known, had articulated nymphal wings (a well During the second phase, (fig. 4, Recent), preserved forewing not fused with the tergum the pre-adult wings in both Paleoptera and is shown on fig. 48). In one paper Sharov (’57a) Neoptera became completely immobilized and described a continuous ontogenetic series of streamlined in a protected position. This was nymphs and subimago-like nymphs showing achieved in two different ways: (1) In Paleop- that their development lacked the metamor- tera (fig. 46:a, Recent) and in exopterygote phic instar. With the probable ancestors being Neoptera (fig. 46:b, Recent) the wings were definitely ametabolous, the Endopterygota de- fixed and fused mesally with the terga, and veloped their “complete” metamorphosis di- the wing integument was thickened. The rectly from the very primitive and confluent cuticular, tubular venation ceased to be useful series of plecopteroid immatures which had and became vestigial, so that only traces of freely movable wings and lacked metamor- former veins occur as weak cuticular ridges on phosis. the wing pads of modern nymphs (fig. 29). The The postero-lateral orientation of nymphal blood lacunae representing the venation were wing pads in both Paleoptera and exop- submerged deeper into the pad, so that they terygote Neoptera occurred independently became well protected on both sides by the epi- and in parallel. First, the wings were indepen- dermis (fig. 4). The surface of the wing pads dently streamlined and directed backwards in was reinforced by cuticular rugosities, hairs, both groups, but by different means: one by a and tubercles. (2) In endopterygote Neoptera “nymphal wing bend’ (figs. 6, 311, the other (fig. 46:b’, Recent) the immobilization and by a pivoting third axillary (fig. 35). Then, protection of juvenile wings was achieved by they were immobilized in this streamlined po- their reduction to imaginal discs. These are sition (fig. 46:a, b, Recent). Hence, in spite of simple formative centers of small cells which their notably similar outward appearance, the appear as epidermal thickenings. Imaginal paleopteran and neopteran nymphs of today discs of wings and other adult organs became are as phylogenetically different as are the invaginated under the larval cuticle and their adults. development during the larval stage was sub- Fossil evidence provides an answer to the stantially slowed down. They are recovered in second question posed at the beginning of this full adult size during the prepupal and pupal section: the postero-lateral position of the instars chiefly by cell multiplication (Boden- wing pads in modern insects is secondary and stein, ’50). Invagination of extremely sup- is not homologous in Paleoptera and Neoptera. pressed juvenile wings was the key character The ontogenetic stages of Pterygota have fol- which gave a monophyletic start to a new suc- lowed a different alar evolutionary pattern cessful neopteran group, the Endopterygota. than the adults, because they have been ex- As proposed by Adams (’581, there is a rela- posed to different survival problems and dif- tionship between these and the plecopteroid ferent selective pressures (fig. 46A,B, upper line. It can be found in wing venation (figs. half compared to lower half). 9A,B), setation, and in the presence of the fur- casternum and of the sternal articulation of Primitive position of wings in adults the coxae. Here it is believed that endop- The phylogenetically primitive position of terygotes were derived from some unknown adult wings at rest in early Pterygota is still a family of plecopteroid Protorthoptera which matter of dispute. A popular hypothesis of 86 JARMILA KUKALOVA-PECK

Bekker (’52),developed by Sharov (’661, Woot- ondary to the fact of flexing itself and belongs ton (’76) and Rasnitsin (’76, ’77) suggests that to a lower phylogenetic category. the oblique-posterior position of the wings is It should be noted, however, that the almost primitive and that it echoes the orientation of homonomous character of the wings and the “paranota” in the hypothetical first “gliding” unfoldable anal area, as they occur in Pa- Pterygota. Paoliidae, the first recorded ptery- oliidae, are definitely primitive characteris- gotes whose wings at rest are oriented tics for the Neoptera as such, and they are obliquely-posteriorly, were referred by Sharov demonstrated in the fossil record. They have (’66) to a separate cohort “Protoptera,” which been inherited by Paoliidae from the immedi- I think has no basis in reality. Protoptera sup- ate ancestors of Neoptera, the early Paleop- posedly represent the most primitive ptery- tera, and were carried over almost unchanged gote group with a flying capability, from to primitive living Endopterygota (i.e., Mega- which both paleopterous and neopterous con- loptera). This fact is viewed as valuable evi- ditions developed. In Paleoptera, the wings dence that the endopterygotes are derivatives “lost” the ability to draw back and became from an early neopteran stock. Thus, the constantly spread out at the sides; in Neop- postero-laterally oriented wings of the earliest tera, the wings gained the ability to flex com- known Neoptera (Paoliidae) and several other pletely backwards over the body. families of Protorthoptera are seen as docu- There is no serious doubt that Paoliidae menting the opposite of what Sharov (’66) and are extremely primitive in having nearly others believed: they represent the early stage homonomous wings with small, completely in the development of neoptery from the more unfoldable anal areas. However, their vena- primitive, ancestral paleoptery. tion carries all neopterous features discussed According to Rasnitsin (’761, palaeodictyop- in the first section of this paper. The question teran and all early pterygote nymphs could is this: is the position of flexed wings to be probably “flex” their wings backwards; he considered phylogenetically as more impor- regarded this as a primitive feature. This tant than the fact itself offlering? First of all, assumption is not supported by the arrange- the postero-lateral “paoliid” position seems to ment of pteralia in the primitive palaeodict- be quite common in families in the primitive yopteran hinge, which lacks both a basal fold Paleozoic order Protorthoptera, in which the and third axillary sclerite in the pivoting posi- neopterous nature has never been questioned. tion (figs. 6a-c, 45A,B). Only the angle of the flexed wings is variable The concept of a primitive, oblique-posterior but the wing-tips are often not overlapping position for the wings in early Pterygota is at- hut pointing postero-laterally. Resting Pro- tractive to the supporters of the paranotal torthoptera are even reconstructed this way theory and to the seekers of a straight-forward by Sharov himself (fig. 33). Other “paoliid” explanation of nymphal wing pad orientation orientations of wings have been gained sec- in Recent insects. As documented in this ondarily in advanced insect groups like flies, paper, however, this reasoning is based only some moths and some caddis flies. The posi- upon an outward resemblance, and this is tion of the resting wings varies; e.g., in moths, foreign to phylogenetic thinking and does not on a subordinal level, from roof-like to oblique find any support in the fossil record. The posterior and even to overlapping. The only arrangement of the sclerites in the newly de- difference in the wing position between scribed primitive articular region of ancient ancient Paoliidae and modern Megaloptera is Paleoptera (fig. 45A), with two simple, paral- that in Megaloptera a very small part of the lel rows of pteralia lined up along the straight anal area (proximally from 2A) is folded under hinge, clearly indicates that the simplest pos- the wings, while in Paoliidae it is not. Other sible wing-articulation was paleopterous. As than that, both groups have equally shaped observed in Recent Paleoptera, the third axil- wings with small anal areas, and their alar lary is a small sclerite divided from PNP only angle is the same. Clearly, the angle of the by a suture (fig. 45B). The neopterous V- wings at rest does not rank highly in phyloge- shaped arrangement of pteralia is much more netic significance and is correlated mainly sophisticated; it can easily be derived from with the wing-shape and with the quality of the primitive paleopterous hinge by shifting the anal area (rigidity, size, foldability, etc.). the third axillary into the pivoting position. A Therefore, the particular position of the wings reverse direction of development, or even the at rest is seen here to be sequential and sec- attempt to derive both arrangements from INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD 87 some kind of intermediate ancestral type of Peck and Peck, ’761, Protorthoptera (Sharov, articulation, as proposed by Sharov (’66) and ’57a, ’66) (figs. 48,49; and undescribed ma- Wootton (’761, is unrealistic. The problem will terial), and Miomoptera (Sharov, ’57b). The be discussed and documented in more detail in number of instars was probably greater than a subsequent publication. in any group of modern insects and develop- Clues to the phylogenetically primitive posi- ment was characterized by a slow and tion of pterygote wings are also available in sequential increase in wing size (Sharov, the morphology of living insects. It is re- ’57a). The change of “younger” instars into capitulated in the earliest wing development “older” instars and of those into “imaginal” of generalized modern insects as described by instars was confluent (Kukalova-Peck and Tower (’031, Durken (’231, and Bocharova- Peck, ‘76; and undescribed material), (fig. 6, Messner (’59,’65). In fact, all nymphal wings 30) and it is quite likely that moulting in Pterygota, in Paleoptera as well as Neop- continued even after the insects reached tera, are at first oriented laterally, i.e., in the maturity, as in living Apterygota (Sharov, primary, paleopterous position (fig. 36). This ’57a). circumstance quite likely reflects the paleop- How does this evidence of ametaboly, found terous character of early Pterygota. The ex- in several lines of Paleozoic pterygotes, relate planation as to why the small wings in the to the probability of the multiple origins of young nymphs would recapitulate the actual metamorphosis? In phylogenetic terms meta- phylogeny while the larger wings in older morphosis is defined as a restoration to the nymphs do not, is seen to be quite simple: im- adult of features that selection has suppressed mediately after evagination and during their in the immature (Wigglesworth,’50) (namely migration towards the tergum, the wing buds the retarded structural growth of wings, the (fig. 36) are too small to interfere with move- suppressed wing articulation, the abolished ment or any other activity. Therefore, no venation, etc.). One (in Paleoptera and exop- adaptive trend (other than a merging of the terygote Neoptera) or two (in Endopterygota) number of instars) alters their natural phylo- metamorphic instars bring all these struc- genetic position. tures back into working condition. Since the The generally more primitive nature of fossil evidence records that all known Paleoptera is also reflected in the well known Paleozoic Ephemeroptera were ametabolous, fact that Paleoptera share numerous charac- whereas all of today’s mayflies are metabolous ters with Apterygota which they do not share and have the metamorphic instar, the ability with Neoptera, and which Neoptera do not to metamorphose could not have been in- share with Apterygota (Snodgrass, ’35). herited from the ancestor, but was instead gained in mayflies in the time period between Onset of metamorphosis the Paleozoic and the Quaternary. A similar All Recent pterygotes are subject to meta- type of simple deduction can be applied to morphosis (defined as given in the INTRODUC- other evolutionary lineages, i.e., to Odonata TION) which evolved as a consequence of the (in spite of the fact that fossil immatures have immobilization and suppression of nymphal not yet been found), under the premise that wings. Metamorphosis compensates for all Odonata, as well as Ephemeroptera, Palaeo- secondary changes in wing size, venation, and dictyoptera, Megasecoptera and Diaphanop- articulation which mainly occurred during terodea, descended from a common paleop- Postpaleozoic ontogenetic development. In the terous ancestral stock. The fossil evidence Paleozoic, nymphal wings of all ancestral in- shows that Paleozoic Ephemeroptera, Palaeo- sect groups were primitively articulated (not dictyoptera and Megasecoptera lacked meta- fused) to the tergum, had tubular venation morphosis, a condition which is generally con- and were functional. Their size increased sidered to be primitive for Insecta. Hence, the gradually at each ecdysis until the adult size ancestral stock was primitively ametabolous. was reached (metamorphosis was not yet nec- To assume that early Odonata developed from essary). This condition has been found in these ametabolous ancestors means also to several families of fossil Ephemeroptera (Ku- assume that the metamorphic instar of Re- kalova, ’681, Megasecoptera (Carpenter and cent Odonata is apomorphic and must have Richardson, ’68; Kukalova-Peck, ’75; and originated between the Upper Carboniferous undescribed material), Palaeodictyoptera and the Quaternary. The mutual relationship (Wootton, ’72; Sharov, ’66, ’71a,b; Kukalova- of metamorphosis in modern Ephemeroptera 88 JARMILA KUKALOVA-PECK and Odonata, consequently, is that of parallel changing form, and before pupation assume evolution. It is here proposed (and it will be the definite position of the pupal wings. The discussed in more detail in a separate publica- pushing of the wings out from the cavity is tion? that metamorphosis in pterygotes origi- often erroneously paralleled with the primary nated independently and several times: at eversion of the wing sack in Paleoptera and least twice in Recent Paleoptera, at least four exopterygote Neoptera. times in exopterygote Neoptera, and only once The ontogenetic development of modern in Endopterygota (fig. 46: A, a, b, b’, U. Endopterygota is here considered to be paral- Paleozoic-Recent). lel with that of Paleoptera and exopterygote The origin of the Endopterygota was the Neoptera. Two different events are recog- last major event in the macroevolution of the nized: (1) The eversion of the wing-sack under grades of Pterygota. However, as shown above, the endopterygote larval cuticle parallels the it happened very early (in the Lower Car- external eversion of the wing buds in the early boniferous?? probably even before the begin- instars of all other insects. This reflects a ning of the known record of the first flying in- major phylogenetic event, the very origin of sects. The presumption that the Endop- the wings and therefore also the origin of the terygota stemmed from very ancient Neoptera Pterygota, which happened some time in the is also supported by their inheritance of some Upper Silurian or Lower Devonian. (2) The early neopteran characters, such as: two passing of the wing outward from the body in homonomous pairs of wings with similar vena- the prepupal instar does not have a parallel in tion; the presence of the subcoxa anterior the other insects. It is part of a phylogenetic (Sc +), MA, and branched CUP; the presence event which was peculiar to Endopterygota: of serial larval abdominal legs (tracheopods); the invagination, subcuticular development, 5-segmented tarsi; etc. Since the supposed and again evagination of larval wings. This ancestral stock of plecopteroid Protorthoptera marks the origin of the Endopterygota, and it in the Paleozoic is repeatedly recorded to be happened much later, sometime in the Pa- ametabolous (Sharov, ’57a, ’661, the so-called leozoic. “complete” metamorphosis of Endopterygota A physiologist might find this new fossil- probably developed from ancestors which based concept of multiple metamorphosis lacked the metamorphic instar. This hypothe- more suitable for an interpretation of his ex- sis might be substantiated, or at least re- perimental data. In the following text an at- flected, in experiments on hormonal action in tempt is made to interpret the metamorphic Recent insects. The conclusion that holome- instar in the light of the fossil evidence. Meta- taboly developed from an ametabolous condi- morphosis of parts other than wings is omitted tion, was previously reached by Sharov (’57a). because, in a phylogenetic sense, they are According to Tower (’031, Bradley (’421, lower in a ranking of character importance Bodenstein (’501, Imms (’64), and Chapman and their changes were subsequent to changes (’691, in the ontogenetic development of in the wings, which are the key character. modern Endopterygota the wings start as epi- Ontogeny of early Pterygota was ame- dermal thickenings which frequently are tabolous and the growth of nymphal wings in already evident in the embryo. In the primi- the whole series of instars was completely tive type, a considerable area of the epidermis sequential. Therefore, the metamorphic instar draws away from the cuticle after hatching; was not needed. It is believed here that this then the dorsal portion of the tissue thickens type of development occurred in all ancestors and is evaginated outwards into the space be- of the main modern lineages: Ephemeroptera, tween the epidermis and the cuticle. A similar Odonata, hemipteroids, orthopteroids, blat- process occurs in more specialized types, in toids, plecopteroids, and Endopterygota. How- which the wing might evaginate inside of ever, as discussed previously, selective pre- pocket-like peripodial cavities. In the larval ssures on pterygote nymphs led to a suppres- stage the wings grow slowly; in the prepupal sion of the size and movability of nymphal stage, when the larva ceases feeding, the wings (fig. 46:A- Recent), while in adults it wings increase rapidly in size due to a rear- emphasized the larger size of the wings and rangement of epithelial cells and pumped-in the capacity to fly (fig. 46:B- U. Paleozoic, Re- haemolymph. The blood pressure finally cent). Eventually the breaking point was pushes the wings out and downwards from the reached, at which metamorphosis became cavity. The wings grow very rapidly while inevitable. This breaking point is believed to INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD 89 have occurred among the series of subimag- all pterygotes were recently summarized by inal instars (figs. 6e,d, fig. 30: last instar; Hinton (’76). Novak (’66) gave a summary of Kukalova-Peck and Peck: fig. 4; and opinions opposite to Hinton’s in which the undescribed material); their intermediately- endopterygote larva is frequently seen as a sized wings made them vulnerable to selective kind of living embryo and extensive des- pressures because they were less capable of embryonization andlor embryonization is flying than adults and also less capable of con- postulated. From the macroevolutionary view- cealing themselves among vegetation or in point, the derivation of a major and old group crevices than younger juveniles. Finally the like Endopterygota was almost certainly primitive sequential ontogenetic series be- caused by some change in the basic pterygote came disconnected at this weak link and an key character, which is the wings. If all three (unknown) series of older nymphs were com- major living groups of Pterygota (Paleoptera, pressed into one (or two in the case of Endop- Neoptera Exopterygota, and Neoptera Endop- terygota) metamorphic instars. On the basis terygota) are compared on the level of this pri- of the fossil record it is not evident how many mary character, all features are perfectly ho- subimaginal instars became incorporated mologizable and the comparison of the events with the imaginal stage, or were compressed in their ontogeny can be made without dif- into the metamorphic instar, or were co- ficulty. If other characters are employed in alesced with the larval stage. In modern the same task, the homologization is difficult Ephemeroptera, the last (?I subimaginal in- or impossible and so is the comparison of the star (the subimago) has persisted to Recent events in the larval stages. (The Berleyse- times as a living fossil and the metamorphic Imms-Polyarkoff hypothesis views the oligo- instar was formed from an unknown number pod, and pre- and post-oligopod larval stages of previous older instars. This fact seems to as phylogenetically important; however, with- support the above interpretation of metamor- in just one order, the Coleoptera, the types of phosis. If the ontogeny of the ancestral stocks larvae vary from campodeiform to apodous, of all modern lineages was primitively etc.). ametabolous, then the formation of the meta- A phylogenetic explanation for the well morphic instars must have occurred sepa- known fact that some Homoptera (whiteflies rately and independently in each line, a proc- and male scale insects) have a quiescent and ess which left room for much variety. pupa-like last nymphal instar is thus not that After the metamorphic instar was estab- there is close relationship between Hemiptera lished, selective pressures towards further and Endopterygota, but that they happen to suppression of juvenile wings probably con- be convergently similar in their metamorphic tinued, and the changes in the metamorphic instars. The only way to explain metamor- instar became genetically more firmly fixed. I phosis in modern insects, then, is by assuming cannot see, from a phylogenetic viewpoint, its multiple and independent origin and paral- any substantial difference between metamor- lel evolution in the major lineages. We can phosis in Endopterygota and the rest of the in- thus account for the many variable ways in sects. It seems to me that there is a perfect which insects metamorphose. parallel between all the phylogenetically Recent imaga sometimes retain many important events concerning the key charac- nymphal features for diverse periods of time. ter-the wings. In Endopterygota, many This happens typically under conditions when imaginal structures originate in the embryo the mode of life is “nymphal,” i.e., secretive, in as epidermal thickenings and later invaginate hiding spaces. Roaches are an example: in the so that they develop in the larval stage com- Paleozoic, only fully winged adult forms of pletely hidden under the cuticle (Bodenstein, cockroaches are known in a rich record of tens ’50).This process includes not only wings but of thousands of fossil specimens. On the other also legs, the thorax, head structures, etc. hand, many modern species become “nym- However, subcuticular development of the phalized” in appearance by reduction or loss of wings is not peculiar to Endopterygota. As their wings and are carrying over the nymphal mentioned by Tower (’03) wing buds of some wing musculature and other features into Orthoptera appear and then evaginate in the adulthood, as observed by Bocharova-Messner embryo under the cuticle and become external (’68). A similar process is known in other in- only after the first ecdysis. Many data sup- sects. In the cricket, Acheta dornestica, as de- porting parallel ontogenetic development of scribed by the same author, some nymphal 90 JARMILA KUKALOVA-PECK characters of the flight apparatus are carried the juveniles. Another common evolutionary over through the metamorphic instar into the trend is that juveniles often follow different imago; adult flight musculature is delayed in adaptational patterns than adults and end up development and becomes functional only in with distinctly different morphologies. For the older adult. This and similar observations these reasons, the most acceptable explana- suggest that the suppression of the flight ap- tion is that juvenile organs of flight became paratus is not restricted to the larval stage and reduced and progressively more and more dif- is not impaired by the metamorphic instar, but ferent from those of the adults because the might occur whenever there is a “need” for a juveniles did not need wings in their habitats flightless condition. It also shows that life in and for their mode of life. This is consistent secretive places might trigger an adaptation with the fossil record and with genetic princi- which, in all probability, was the primary ples in general. In consideration of the possi- cause of the origin of metamorphosis. bility of the reversibility of characters and structures, there is indeed a school that V. Principles of irreversibility and rejects the principle of irreversibility of evolu- irrevocability of evolution tion, as currently defined and favored by While discussing with various entomol- paleontologists and geneticists. This is based ogists the results presented in this paper, I upon occasionally observed events in labora- was cautioned that the articulated attach- tory populations, such as the disappearing and ment of Paleozoic nymphal wings (presently reappearing of certain bristles in flies, hal- known to exist in 5 primitive orders, including teres turning “back” into wings with veins, all known nymphs of Ephemeroptera and heteromorphosis in the regeneration and re- plecopteroid Neoptera) might not be a primi- placement of a lost antenna by a leg, or of tive, but rather a highly advanced condition. halteres by legs, etc. The matter has been As an alternative, it has been repeatedly sug- thoroughly examined by geneticists and their gested to me that the wing pads of modern conclusion is that genetics does not provide the nymphs, which appear as continuous expan- key to the problem of homology, as proven by sions of the terga, might be primitive “par- frequent substitutions of non-homologous anota” directly inherited from unrecorded structures (production of an extra antenna in- (Devonian) ancestral lineages (i.e., that the stead of eye, etc.). De Beer (’711, in a discus- mainstream of wing evolution might have sion of these strange phenomena, takes the bypassed the contradictory Paleozoic fossil stand that homologous structures need not be groups). Another suggestion was that the ar- controlled by identical genes, and notes that ticulation of the wings has even been this highly important fact has been experi- “reversed” in modern nymphs back to the mentally verified. It means that the homology ancestral state of tergal paranota. Both these of phenotypes does not imply similarity of alternatives are completely alien to the basic genotypes. Hence, the same bristle of a fly concepts of phylogeny. First, the evolution of may be controlled by different genes and its structures does not consist of independent “reappearance” does not necessarily prove the changes of organs or traits; what changes is the reversibility of evolution, especially in the genetic system, and the developmental system light of the massive and contradictory evi- rests on it (Dobzhansky, ’70;De Beer, ’71; and dence accumulated in the past two centuries others). I know of no case in the fossil record of by paleontologists. the entire Animal Kingdom where a key struc- A good understanding of the “principle of ture temporarily occurred in ancient juveniles irreversibility of evolution” is basically neces- in a functional and perfected form, while sary for all phylogenetic considerations, in- modern juveniles are left with the ultra-prim- cluding the correct interpretation of insect itive pre-adaptive condition of the same key morphology. Its validity is viewed by genet- structure. The above two interpretations of icists as dependent on the micro- or macro- the fossil and Recent data are clearly against level of the evolutionary changes while the all the accumulated experience of paleon- distinction between them is considered to be tology as well as of genetics. On the other quantitative. The mutation (i.e., microevolu- hand, it is a well known phenomenon that the tionary change) that is only temporarily simplification and reduction of complicated favored by selection is generally believed to be structures, if unnecessary or obstructive to an reversible; the lost combination can be re- adaptive trend, are very common, especially in covered by recombination or back mutation; INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD 91 and the direction of selection may change in a derived prothoracic lobes; and 9. The preser- different environment. By no means, however, vation of residual wing venation and muscula- does this alter the broader fact that as soon as ture in the wing-derived abdominal “gills” of a macrostructure is genetically established, Ephemeroptera. evolution does not double back on itself to These ancestral conditions which are ex- return to ancestral states. This fact is basic for pressed in wing morphology and development evolutionary biology and is complemented by are neither abundant enough nor sufficiently the important “principle of irrevocability of understood to serve as a secure basis for a com- evolution,” which is: The influence of the plete explanation of wing origin. However, ancestral condition is not fully lost in de- any real reconstruction of this important scendent groups. In phylogenetically sound re- event, as well as the correct interpretation of constructions of lineages, one should expect the morphological structures in modern in- both principles to be expressed. sects, are bound to include an adequate and in- Applied to the particular case of nymphal ternally consistent explanation for all these wing articulation, the “principle of irrever- interrelated features and phenomena. sibility’’ is evident in the following sequence VI. Wings and taxonomy of features: 1. The wing articulation arose only once (monophyletically) in the Ptery- Differential diagnosis of Paleoptera gota, as documented by homologous articulary and Neoptera sclerites within the whole taxon; 2. The artic- In the current entomological literature, ulation was lost separately and independently there is a remarkable uncertainty about in most phylogenetic lines, as documented by which characters reliably separate Paleoptera the different times at which they were lost, from Neoptera. This question has to be ap- shown by the fossil record; 3. The loss of the proached on a phylogenetic basis, by following nymphal wing articulation was followed by the sequence in which the characters de- the simultaneous and independent appear- veloped. ance of metamorphosis, as documented by Paleoptera and Neoptera are sharply sepa- fossil evidence. Thus, the articulation that rated by three ancient characters: the pres- ceased to be useful for the juveniles was sup- ence or absence of wing flexing; the intensity pressed, while the same articulation that was and regularity of primitive vein corrugation; essential for the adult was again released dur- and the arrangement of the pteralia. Never- ing metamorphosis. Both processes are hor- theless, none of these features, as such, is di- monally controlled and the manipulation of rectly diagnostic. the condition of the wings and of the articular Wing flexing. The ability to flex the wings structures through hormonal action is a phy- backwards over the abdomen at rest has de- logenetically new (or younger) function for veloped twice, in Neoptera, and in one order of the already existing endocrine system. Paleoptera, the Diaphanopterodea. There is a The complementary “principle of irrev- common misunderstanding about the phyloge- ocability of evolution” in the wings of modern netic significance and validity of this flexing nymphs is clearly demonstrated by: 1. The for the separation of Paleoptera and Neoptera, remnants of a once functional venation re- based on casual observations of paleopterous maining as cuticular ridges on the nymphal Odonata, namely damselflies. They seem to wing-pads; 2. The fact that the wing anlagen show that they can flex their wings backwards always evaginates above the spiracle; 3. The over the abdomen, thus being “neopterous,” migration of the wing-buds dorsally towards and seem to give the lie to the reality of the the tergum; 4. The generally lateral Le., paleopterous category. However, careful ex- paleopterous) orientation of all young wing- amination of damselflies reveals that the pos- buds; 5. The fusion of the wing-buds with the teriorly directed position of their wings (while lateral margin of the tergum; 6. The preserva- at rest) is achieved by a change in the tion of the dual (i.e., tergal and alar) origin of nevertheless paleopterous thoracic construc- sclerites forming the different sides of the tion. The thoracic segments are displaced hinge; 7. The preservation of the subimaginal from a vertical position to a nearly horizontal instar in Ephemeroptera as witness to a previ- one, so that the wings become posteriorly di- ous and generally present incremental and rected. In this way the anterior margin of the ametabolous ontogenetic development; 8. The wing at rest is placed dorsally and upwards preservation of a reduced hinge in some wing- with respect to the body, rather than being 92 JARMILA KUKALOVA-PECK pivoted and placed laterally and near the in- absence of wing flexing nor the corrugation of sect’s ventral surface as in the neopterous con- central alar veins, but the particular charac- dition. Thus, damselflies only lift their wings ter state of these features, as phylogenetically upwards in the same way as modern mayflies. evaluated, securely separate the Paleoptera This movement is simple and does not require from the Neoptera. Similar modifications de- any complicated mechanism, and is not con- veloped at least twice in each group, but by vergent to neoptery. The neopterous sclerite different means, thus giving a typical exam- mechanism is, in comparison, very complex ple of convergence. Therefore, the establish- and resulted from a more profound adapta- ment of key characters between Paleoptera tional process. and Neoptera is somewhat difficult. I suggest Neoptera were derived from the ancestral that the position of the basal fold within the paleopterous stock with short mouthparts at a hinge (in Neoptera) or distal to the basi- very early period in insect evolution, by de- venales (in the convergent Paleoptera) can be velopment of a wing-flexing ability through a used as a distinctive feature whenever there is pivoting of the third axillary sclerite. Their a need to cover both extinct and extant orders. basal fold for wing flexing is located directly Pteralia. For Recent Neoptera, the V- within the hinge line; the veinal corrugation in shaped arrangement of the tergal sclerites the central wing area (Rs, MA, MP, CuA) has with the median sclerite and the third axillary become successively less distinct. Diaphanop- sclerite forming the V-angle, and the presence terodea (fig. 27) were derived later, directly of a pivoting third axillary, are the phyloge- from the extinct paleopterous order Palaeodic- netically based and distinctive basic charac- tyoptera with elongate haustellate mouth- ters which are both apparent and simple. I do parts, after the true neopterous lineage was not recommend using this differentiation for established. They are stratigraphically the extinct orders, because we do not know younger than Neoptera (according to present whether or how the third axillary was engaged fossil record). Their flexing mechanism is not in flexing in the paleopterous Diaphanop- known, but it must have been different from terodea. An unfailingly distinctive feature for that of the Neoptera, since their wing-flexing the Recent Paleoptera is the extensive fusion basal fold was located distal to the basivenales of the basivenales into a large basivenal plate and not within the hinge; the corrugation was (sometimes called the “axillary plate” in not affected by wing-flexing and remained Paleoptera, or “radioanal plate” in Odonata, typically paleopterous (Kukalova-Peck, ’74a). and “median plate” or “subcostomedian Corrugation. The “typical” accentuated plate” in Ephemeroptera) ; the size of basive- corrugation of Paleoptera tends to become les- nales in Neoptera is always comparatively sened in some specialized Recent Ephemerop- negligible. Another feature of the Paleoptera tera. According to Edmunds and Traver (’54) is the position of the median sclerite; this is the corrugation in the radio-medial area is always located posterior, or postero-proximal being suppressed in the Palingeniidae, Be- to the second axillary sclerite, but is never dis- hingiidae, and Oligoneuriidae. This occurs by tal or postero-distal to it, as in the Neoptera. a migration of the concave veins to the vicinity of the convex veins, or by a near Monophyly and parallel development fusion of the concave veins with the convex in Pterygota veins (very weak concave veins lie next to the As generally accepted by paleontologists convex veins or in the fold beneath the convex and pointed out by Hennig (’661, the main veins). Oligoneuriidae have developed a scull- contribution of the fossil record to recent clas- ing type of flight which is, according to these sification is that it makes more possible the authors, responsible for the tendency to sup- correct classification of the categories of re- press the fluting. The “typical” condition of semblance between characters, by revealing the centrally located veins in most modern convergence and symplesiomorphy. The phylo- Neoptera is flat (not corrugated) but is slight- genetic system classifies organisms according ly corrugated in some primitive living Neop- to their degree of phylogenetic relationship. In tera and in fossil Protorthoptera, and highly this system, the possession of at least one corrugated in specialized Recent Endop- derivative ground-plan character (basic apo- terygota. morphic character) is a precondition for a It is thus clear that neither the presence or group to be recognized as a monophyletic INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD 93 group. All available fossil evidence testifies nymphal tubular venation to surface ridges, that the basic apomorphic character (the key in modern Paleoptera and Neoptera-Exop- character of Mayr, ’63) for Pterygota is the terygota; reduction of prothoracic and termi- presence of wings. These induced the origin of nal abdominal spiracles, in Pterygota; chang- Pterygota, but also the origin of Neoptera, and ing in-and-out pulsation of blood into a Endopterygota, in three subsequent steps of loop-like flow, in the wings of Paleoptera and wing evolution. Neoptera; development of special metamor- Here, I propose that all major evolutionary phic instars to compensate for reduction steps with respect to wing development hap- and immobilization of nymphal wings, in all pened not in the adult, but in the juvenile modern Pterygota. stage, as follows: 1. Pterygota originated The use of both convergent and symple- monophyletically from a common ancestor of siomorphic characters for differential diag- both Archaeognatha (including Monura) and nostic purposes creates an artificial polyphyly Thysanura, through the origin of a paleop- and undesirable “parasystems” (pseudophylo- terous type of wings; 2. Neoptera originated genetic systems), which give the false impres- monophyletically from the early Paleoptera sion that it is arbitrarily possible to classify through the development of wing flexing by a insects by means of several types of systems. pivoting third axillary sclerite; and 3. Endop- In reality, there is only one possible system terygota originated monophyletically from which reflects the actual phylogenetic path. the generalized plecopteroid-type of Pro- All other classifications (i.e., that of Lemche, torthoptera, through the withdrawal of de- ’42) are of necessity based upon outer resem- veloping wing buds into subcuticular pockets. blance of characters which often has very lit- In the first and second step, the innovation in tle to do with the phylogeny. Examples of juvenile wing characters was carried on to the parasystems are the following: classification adults. All three steps had tremendous impact of insects into Ametabola and Metabola; of on the radiation, dispersal, survival, and dis- Pterygota into Hemimetabola and Holo- tribution of the particular new group (fig. 46). metabola; of Pterygota into Opisthoptera The other characters, which became diver- (= Ephemeroptera and Neoptera) and Plagi- sified before or after each major event, fol- optera (the rest of Paleoptera); and of insects lowed various mosaic and parallel patterns. into Monocondylia and Dicondylia, etc. These Hence, the accompanying characters, like the parasystems are based upon metamorphosis, state of the anterior mandibular articulation, orientation of nymphal wing pads, and stage are not decisive in judging the phylogenetic of development of the anterior mandibular ar- category of the three major respective groups ticulation. I believe that all these features de- (but may be helpful as being indicative of it). veloped several times, independently in both The following wing characters, sometimes Paleoptera and Neoptera, and do not represent previously regarded as important for classifi- the basic apomorphic characters (key charac- cation, have been documented by fossil evi- ters) in Pterygota. dence to be parallel, convergent, or symple- The classical example of artificial polyphyly siomorphic: wing-flexing, in some ancient is the separation of Odonata from other Paleoptera (Diaphanopterodea) ; diminishing Paleoptera, or even from all Pterygota of wing corrugation, in some Recent Paleop- (Mackerras, ’67; Kristensen, ’75; Matsuda, tera (Ephemeroptera); deepening of wing cor- ’65, ’70, ’76) on the basis of a misreading of rugation, in higher Diptera and some Hymen- secondary apomorphic characters such as: optera; immobilization of all pre-adult wings, “missing” veins, the specialized mechanism of in Pterygota; fusion of nymphal wing pads mating, the “lack” of a telsonal appendix, the with terga, in Paleoptera and Neoptera-Exop- presence of a dicondylous mandible, details of terygota; reduction of the size of pre-adult head structure, derived morphology of the wings, in Pterygota; bending of the nymphal thorax, “different” pteralia, tracheation, “pe- wing-pads into the oblique-backward position, culiar” orientation of nymphal wings, etc. in Paleoptera; twisting of the nymphal wing Most of these differences have been discussed pads about their points of attachment, in here on phylogenetic grounds or are found to Odonata and Orthoptera; locking of the fore be homologous with features of other Paleop- wings in the outstretched position for gliding, tera through the “closing the gap effect” of in various Neoptera; reducing ancestral the fossil evidence and will be described in 94 JARMILA KUKALOVA-PECK future publications; others are currently be- paleontology and evolution, and of the 20 ing interpreted as homologous in a large-scale years of encouragement and support that he comparative morphological study (E. L. has given to my work. This does not mean that Smith, California Academy of Sci., personal he agrees with all the conclusions presented communication in 1976). here. My husband, Dr. Stewart B. Peck (Carle- To some entomologists it might seem to be ton University, Ottawa), also made this work asking too much to believe that so many insect possible through his help, support, and encour- characters originated and developed at dif- agement. I am specially indebted to Doctor M. ferent rates and achieved by parallel evolu- C. Parsons (University of Toronto), Mr. A. tion in separate lineages such a remarkably Downes, Doctor J. W. Arnold, Doctor J. F. high degree of morphological resemblance. McAlpine, and Doctor E. Lindquist (Biosys- However, this type of evolution is frequent tematic Research Institute, Ottawa) as well throughout the Animal Kingdom, and espe- as to Doctor H. Howden (Carleton University, cially in insects (Mackerras, '67; Hinton, '55; Ottawa), and Doctor V. Pokorny (Charles Uni- and others). Indeed, parallel development, as versity, Prague), for reading earlier drafts of an alternative to homology, is a more signifi- this paper and for suggesting significant cant agent in evolution than has been recog- improvements. Doctor E. L. Smith (California nized. Academy of Sciences, San Francisco) made a De Beer ('71) analyzed parallelism in which number of very useful observations. Doctor F. a complicated mechanism (such as the Sehnal (Czechoslovak Academy of Science, tracheae in Arthropoda) evolved repeatedly Prague) provided consultations on metamor- and separately within groups of organisms phosis which contributed significantly to my which are related on an embryological and conclusions. morphological level. He pointed out that cer- The fossil material used in this paper was tain parallelism, called by him latent homol- made available for study through the courtesy ogy, conveys the impression that beneath the of the following people and institutions: Doc- homology of the phenotype, there is a genet- tor V. Pokorny, Charles University, Prague; ically based homology which can provide fur- Doctor F. M. Carpenter, Museum of Compara- ther evidence of affinity between the groups. tive Zoology, Harvard University, Cambridge; Many cases of parallelism are most likely ge- Doctor E. S. Richardson, Jr., Field Museum of netically based and are thus, in a sense, ho- Natural History, Chicago; Doctor C. L. Rem- mologous. Similarities in two or more genetic ington and Mrs. J. S. Lawless, Peabody lines that develop in parallel are channeled Museum, Yale University, New Haven; Doc- mainly by a common ancestry and not prin- tor B. B. Rohdendorf, Paleontological Insti- cipally by environmental selective pressures tute of the Academy of Sciences, Moscow; (which cause convergence). Compared to this, Doctor J. P. Lehman, Museum dHistoire only those features which can be traced back Naturelle, Paris; and Doctor P. E. S. Whalley, to the same (or an equivalent) feature in the British Museum (Natural History), London. common ancestor of a particular taxon are ho- The study was aided by three books on in- mologous (Mayr, '63). sect morphology by Doctor R. Matsuda The importance of parallelism and its (Biosystematic Research Institute, Ottawa) impact on the evaluation of characters is not which opened the door to the literature on the yet fully recognized by comparative mor- subject. To Doctors J. Moore and K. Hooper phologists and taxonomists. At present, the (Department of Geology, Carleton University, prevailing philosophy seems to be that related Ottawa) I am very thankful for the provision and descendent Le., homologous) structures of working space and research facilities. are all those which: 1. look the same, 2. have Field, museum, and laboratory studies have similar position, attachment, etc. and 3. are been supported personally by my husband, by being served by similar musculature. One goal grants to Professor F. M. Carpenter from the of this paper has been to show that the possi- US. National Science Foundation, and by ble kinds of relationships can be more subtle operating grants to me from the Canadian and much more varied than this. National Research Council, and the Penrose Fund of the Geological Society of America. ACKNOWLEDGMENTS This paper is dedicated to Professor F. M. LITERATURE CITED Carpenter (Harvard University, Cambridge) Adams, A. 1958 The relationship of the Protoperlaria in recognition of his contributions to insect and the Endopterygota. Psyche, 65 (4): 115.127. INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD 95

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A, anal vein DE, dorsal epidermis MA, media anterior ps, prescutoscutal sulcus Te. tergum ah. anal brace area DL, dorsal layer me, median lobe R, radius Tp. leg trachea AC, axillary cord En, endocuticlc M1, metamorphic instar RI, radius anterior Tsp. spiracular trachea am, anterior margin Es, episternum mm, middle membrane Rs, sector radii. radius urn, subcoxo-coxal muscles ap, apodemal pit Ex, exocuticle MP, media posterior posterior UM, muscles bc, basicostale f, fat body n. notal median sclerite s, suralare v. vein bm, basement membrane g, gonad ne, abdominal nervous cord Sc, subcosta VE. ventral epidermis br, basal brace G. gut no, notch sct, scutoscutellar sulcus VL, ventral layer bv, basivenale h, hinge line p. prealare sex, subcoxa Vs, dorsal vessel C, costa H, hinge pa, paranotal sulcus sp, spiracle W, wing (wing anlagel cr, cross vein HA, haemocoel pm, postmedian lobe SV, spurious vein 1,2,3,4, first, second, third Cu, cubitus IV, intercalated vein PNP, posterior notal wing t, tegula fourth axillary CUA, cubitus anterior k, patella process T, longitudinal main sclerite CUP, cubitus posterior m, median sclerite pp. posterior arm of prealare trachea +, convex vein cx, coxal area M. media PRA, prealar bridge Tb, gill trachea - . concave vein

PLATE I

EXPLANATION OF FIGURES

1 Prothoracic winglets (arrow) in primitive Palaeodictyoptera, which were not fused with the prothorax, as indicated by their detached, upward folded, and superimposed position. The patella (kJ is distinct from the tibia. Lycocercus goldenbergz; Upper Carboniferous, France. After Kukalova (‘69-’70).

2 Tubular, corrugated, and pigmented venation in a paleozoic nymphal fore wing. Protereisrna sp., Ephemerop- tera; Lower Permian, Oklahoma. After Kukalova (’68). + and -, convex and concave veins.

3 Dorsal view of cleared whole mount of wing pad showing blood lacunae (channels stippled, C, Sc, R + M, Cu, A) that preceed uenation, in wing pads of modern nymphs. Pteronarcys proteus, Plecoptera; hind wing of fourth instar; Recent. After Holdsworth (‘42).

4 Cross section through z- - - - z level of figure 3. Lacunae (Cu + AJ form only in the dorsal epidermis (DEJ; once within the wing pad, each lacuna (R + M, Sc, C) is completed by application of ventral epidermis WE). Lacunae are deeply sunken, and are not connected with wing pad “venation” which is only composed of cuticular ridges. After Holdsworth (‘42).

5 Primitive corrugation in paleopterous wing, formed by alternating veins. Convex veins iC +, RI +, etc.) are formed only in dorsal layer (DL),concave veins (C-,Sc-, Rs-, etc.J only in ventral layer (VL).Siphlonurussp.. Ephemeroptera; wing, part of a cross section; Recent. After Edmunds and Traver (‘541, the costa rein- terpreted as fusion of C + and C - according to new fossil evidence. INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD PLATE 1 Jarmila Kukalova-Peck -

RI +

C

02

5 PLATE 2

EXPLANATION OF FIGURES

6 Ametabolous ontogenetic development characteristic for Paleozoic Paleoptera: young nymphs (ad had their winglets curved backwards by the nymphal wing bend (arrows); in subimago-like old nymphs id,e) the wing axis was straightening gradu- ally until imago (f) resulted. Convex hinge (HI ran between concave paranotal sulcus (pa) and flat basivenales (bv). Palaeodictyoptera: a. Rochdalia parkeri, young nymph; b. Idoptilus onisciformis, nymph; c. Tschirkovaea sp., nymph, hind wing; d. Stenodic- tya perriera, subimaginal nymph, fore wing; e. Stenodictya perrieri, subimaginal nymph, fore wing; f. Stenodictya agnita, imago, fore wing; Upper Carboniferous, Europe. a,b, after Wootton (‘72); d, f, after Kukalova (‘69-’70); c, after Sharov (’71b) and Rasnitsin (‘76); slightly altered.

100 INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD PLATE 2 Jarmila Kukalova-Peck

6

101 PLATE 3

EXPLANATION OF FIGURES

7 Early paleopterous wing with completely preserved primitive set of alternating convex and concave veins, sectioned near the base to show vein pairs of the costa (C+, C-I, the subcosta (Sc+, Sc-1, and the anal (1A+, 2A-I which are usually obscured or inconspicuous in other insects. Specimen PE 16138, Field Museum, Chicago, primitive Homoiopteridae, Palaeodictyoptera. Upper Carboniferous, Illinois. Original. A Cross section through the anal brace area (ab, shaded). B. Cross section slightly distal from the anal brace (abrl

8 Cross section through modern paleopterous wing with reduced set of alternating convex and concave veins. Aeshna sp., Odonata: fore wing, distal from the arculus; Recent. Original.

9 Cross section through similar hind wings of: A. Lernmatophora typa, plecopteroid Protorthoptera; Lower Permian, Kansas. B. Sialrs mohrr, Megaloptera; Recent. Both wings share an Rs + MA which is almost levelled with MP. and CuA sunken into an aerodynamic trough. After Adams ('58).

10 Cross section through elytron showing corrugation diminished by excessive cuticularization in both dorsal and ventral layers. Sc weakly preserves its concave position. Prionus sp., Cerambycidae, Coleoptera: Re- cent. Original.

11 Similar section as 10, but Sc has lost its concavity. Eleodes sp., Tenebrionidae, Coleoptera; Recent. Original

12 Fore wing of a higher fly with accentuated corrugation supplemented by a highly convex spurious vein (SVJ.Syrphus balteatus, Diptera; Recent. After Rees ('721, slightly altered, interpretation of veins added (br-brace; cr-cross vein).

13 The same wings as in 12 in cross section. After Rees ('721, interpretation of veins added

102 INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD PLATE 3 Jarmila Kukalova-Peck

C I 8

c sc

D.

103 PLATE 4

EXPLANATION OF FIGURES

14 Most primitive known fossil prothoracic winglet, attached only at a rudimented hinge (H) and basivenales (bv). Venation is fan-like and weakly corrugated. Stenodictya pygrnaea, Palaeodictyoptera; Upper Carboniferous, France. After Kukalova (‘69-’70), new observations added.

15 Transformed prothoracic winglet of Paleozoic Ephemeroptera which became fused with protergum. Protereisrna permianurn, adult; Lower Permian, Kansas. Original (based upon specimen 3405b, Museum of Comp. Zoology, Harvard Univ.).

16 Transformed prothoracic winglets of Paleozoic Neoptera which shielded the legs. Specimen 1/1977, Charles Univ., Prague, Protorthoptera; Lower Permian, Czechoslovakia. Original.

17 Transformed prothoracic winglets of plecopteroid Protorthoptera which were strengthened by robust venation and spines covered with setae. Specimen 211977, Charles Univ., Prague; Lower Permian, Czechoslovakia. Original.

18 Transformed prothoracic winglets of a neotropical mantid, with rudimentary hinge (HI and secondary venation. Choeradodinae, Mantodea; Recent. Original.

19-21 Transformed prothoracic winglets of small Paleozoic roaches showing various po- sitions of rudimentary hinge (HI. Specimens 311977, 4/1977, 511977, Charles Univ., Prague; Lower Permian, Czechoslovakia. Originals.

104 INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD PLATE 4 Jarmila Kukalova-Peck

105 PLATE 5

EXPLANATION OF FIGURES

22 Young nymph of Paleozoic terrestrial palaeodictyopteran, the winglets of which were articulated, but ap- parently afunctional (as a secondary adaptation); lateral parts of abdomen were formed by margined sub- coxae (scx), not by "paranota" as previously expected. Rochdalia parkeri: Upper Carboniferous, England. After Wootton ('72). Original reconstruction.

23 Adult female palaeodictyopteran, showing prothoracic winglets attached only at rudimented hinge and ab- domen with margined subcoxae (scx).Stenodictya lohata; Upper Carboniferous, France. After Kukalova ('69-'70).

24 Young nymph of Paleozoic terrestrial palaeodictyopteran with armored and flattened body; the wings are curved backwards and carry pteralia. Idoptilus onisciforrnis; Upper Carboniferous, England. After Woot- ton ("72). Original reconstruction from latex peel. 107 PLATE 6

EXPLANATION OF FIGURES

25 Pterygote abdominal wings. A. Lateral schematic view of middle abdominal segment of modern ephemerid nymph; cleared, showing subcoxo-coxal muscles (uml, left gill- plate (wing) with veins (v) and strengthened anterior margin (am), articulated by fused basivenales (bv) between the margined subcoxa (scx) and the tergum (Tel. Cox- al area (cx) weakly indicated, spiracular anlage (*, sp) not externally discernible. Original. B. Abdominal wings as found in primitive fossil Protorthoptera. Venation is very weakly preserved. Quercopterum decussatum, specimen 4311963, Charles Univ., Prague, two of the anterior abdominal segments; Lower Permian, Czechoslovakia. Original observation in 1977, wings on the left side reconstructed.

26 Differences in fore and hind wing venation and corrugation of Per~planetaarnerz- cana, Blattodea. Veins are convex (+I, concave (-), or leveled (unmarked); Sc (+I is reduced to a weak fold; only concave M is labeled as MP. In the tegmen, most veins are leveled and branches of RI, Rs and part of M form an inseparable complex. In the hind wing 1A sends off anteriorly one to two branches; veins are corrugated near the base but are mostly leveled distally; Recent. Original.

108 INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD PLATE 6 Jarmila Kukalova-Peck

25 A

LUH sc+ SC- RI+ Ll I MB RS- RI+

M

rblP-

I I 2A IA + 26

109 PLATE I

EXPLANATION OF FIGUKES

27 Besides Neoptera, wing flexing occured in one extinct order of Paleoptera, the Diaphanopterodea. Phaneroneura sp.; Lower Permian, Czechoslovakia. Original re- construction from a complete specimen.

28 Typical Paleozoic mayfly, older nymph. Wings were curved backwards, articulated, and probably used for underwater rowing; prothoracic winglets were fused with pro- tergum. Abdomen was equipped with nine pairs of veined wings. Legs were long, cur- sorial, with five tarsal segments. Protereismatidae; Lower Permian, Oklahoma. After Kukalova ('68).Original reconstruction from a complete specimen.

110 INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD PLATE 7 Jarmila Kukalova-Peck PLATE 8

EXPLANATION OF FIGURES

29 Metabolous development in Recent primitive mayflies (Siphlonuridae), shortened and schematized. Wing pads are secondarily fused with the terga and suppressed in size; articulation, venation, and adult size are recovered during the metamorphic instar (MI). Original.

30 Ametabolous development typical for Paleozoic mayfly nymphs (Kukaloviidae). Wings were neither fused nor suppressed in size, but were articulated, veined and functional in forward motion. The wings were streamlined by being curved backwards by a nymphal wing bend (arrows) which gradually straightened in each subsequent older instar until the alar axis became perpendicular to the body in the adult (not shown); the metamorphic instar was not present because it was not “needed”; Lower Permian, Czechoslovakia. After Kukalova (‘68). Original reconstructions from actual specimens. 113 PLATE 9

EXPLANATION OF FIGURES

31 Ametabolous paleopteran, terrestrial nymph with articulated wings curved back- wards at nymphal wing bend (arrows) for easier movement; posterior margins of terga carried long integumental projections covered with setae. Mischoptera doug lassr, Megasecoptera, young nymph; Upper Carboniferous, Illinois. After Carpenter and Richardson (‘68). Original reconstruction.

32 Ametabolous paleopteran, adult (integumental projections are not figured). Mischoptera mgra, Megasecoptera; Upper Carboniferous, France. After Carpenter (‘51).

33 Ametabolous neopteran, terrestrial nymph with articulated and movable wings which were not fused with the tergum as in modern metabolous Neoptera. Atac- tophlebia terrnitoides, plecopteroid Protorthoptera; Upper Permian, Urals. After Sharov (’57a).

34 Ametabolous primitive neopteran adult as they are sometimes found with in- completely flexed wings shown by the non overlapping of the wing tips. Syluiodes perloides, plecopteroid Protorthoptera; Lower Permian, Urals. After Sharov (‘68).

35 Paleozoic nymph of a neopteran with wings on three thoracic and ten abdominal seg- ments. Specimen 8592 ab, Museum of Comp. Zoology, Harvard Univ., young nymph, probably plecopteroid Protorthoptera; Lower Permian, Kansas. Original reconstruc- tion after a complete specimen (fig. 48).

114 INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD PLATE 9 Jarmila Kukalova-Peck

32

33

31 115 36 Ontogenetic development of wing (W! in modern dragonflies showing: an incipient epidermal thickening just above the spiracle (spl in instar 1 and 11; evaginated wing bud shifthg towards the tergum (Tei in in- star V; and posteriorly curved wing pad fused with the tergum resembling "paranotum" in instar VIII. Lihellula quadrzmaculata, Odonata; Recent. After Bocharova-Messner ('59).

37 Section through the sixth abdominal segment of first instar nymph of Ephernerrlla gnrta, showing posi- tion of spiracular trachea (Tspi. gill muscle (umi and the anlage of future spiracle (spl: Ephemeroptera; Recent. After Durken ('23).

38 Section through the fifth abdominal segment of fourth instar nymph of Ephemerella zgnita, showing anlage of the gill-plate (W) in relation to the supposed subcoxo~coxalmuscle (urn);Recent. After Durken 1'23).

39 Frontal section through thorax of older nymph of Ephemerella sp., showing spiracular trachea (Tsp! and mechanically closed prothoracic spiracle Ispi; Recent. After Durken ('231.

40 Section through an abdominal segment of nymph offfeptagenia fiaua, Ephemeroptera, showing intermedi- ate position of spiracular trachea (Tsp! between the vestigial leg- ITp1 and gill-(Tb) trachea; Recent. After Landa ('481. E

Q v)

117 PLATE 11

EXPLANATION OF FIGURES

41 Blood circulation at the alar base in modern insects. Anterior veins are opened to af- ferent flow, while posterior veins are sealed by fused membrane (black) and are accessible only to efferent flow; channels with irregular edges represent regions where blood leaks between the basement membranes. Blattella sp., Blattodea; Re- cent. After Clare and Tauber ('421, slightly altered.

42 Parasagittal section of ephemerid thorax at base of fore wing shows fused basivenales (bv) as blood sinus carrying the afferent current, and axillary cord (AC) carrying the efferent current. Heragenia rigida; Recent. After Arnold ('64).

43 Posterodorsal view of the wing base of a libellulid dragonfly showing the basicostale (bc) and the fused basivenales (bv1 as active blood sinuses. Barrier between afferent- efferent flow is the dashed line. After Arnold ('64).

44 Typical loop-like blood circulation in modern insects. Acroneuria arenosa, Plecop- tera. After Arnold ('64).

118 INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD PLATE 11 Jarmila Kukalova-Peck

\ anterior sinus c

sc - R+ CUP-

AC 43 PLATE 12

EXPLANATION OF FIGURES

45 Most primitive known fossil pterygote hinge (in Palaeodictyoptera) (fig. 45A1, and the schematic in- terpretation (fig. 45B) showing homology of all pteralia. The hinge line (h, scalloped lines1 separates serial tergal pteralia It, 1, 2, ml which are slanted mesally into the paranotal sulcus (pa, parallel lines), from serialalar pteralia iC, Sc, R, M, Cu, A) formed by flat, sclerotized veinal blood sinuses. Basicostale iC) func- tionally enters into the convex hinge line (widened for clarity). Tergal pteralia probably originated so that the tergum incised into the five lobes, prealare (p), suralare is). median lobe (me),postmedian lohe (pml, and posterior notal wing process (PNP) separated by a notch (no);only Ephemeroptera and Odonata carry posterior arm of prealare lpp); from the lobes, the tegula (t)and the axillary sclerites (1, 2, m) detached serially along the paranotal sulcus (pa). Tegula and first and second axillary have been previously homol- ogized. The median sclerite (m, nomen novuml of Recent Paleoptera was misinterpreted as the third axil- lary, but, is in fact homologous with the “proximal median plate” of Neoptera. The third axillary (3) in Paleoptera (observed so far only in Recent orders) lies close to the PNP, so that the tergal series is more or less straight. In Neoptera the third axillary (31 separated from the PNP and was placed in a pivotal position so that the series became typically V-shaped. Alar pteralia originated from sclerotized veinal bases, the hasivenales. The hasicostale (C) has been homologized before (as the humeral plate). Sc, R, M, Cu, A, basivenales compose the hasivenal (axillary) plate of Odonata; Sc, R, M hasivenales, the basivenal (median) plate of Ephemeroptera. while the enlarged basicuhitale stays separate, followed by the small basianale. In Neoptera, basivenales are smaller and fuse occasionally into a “distal median plate.” The neopterous V- shaped hinge supposedly was derived from the straight paleopterous hinge demonstrated here, through the third axillary attaining the pivotal position. The lines between pteralia on B. signify: one line - rare artic- ulation. two lines - frequent articulation. Paired apodemal pits (ap) lay mesally from median lobe (me1 Specimen PE 16138, Field Museum, Chicago, and specimen 2, coll. Carr, Univ. of Illinois, Urhana. Homoiop- teridae. Palaeodictyoptera; Upper Carboniferous, Illinois. Original, reconstructed from two specimens.

120 INSECT WINGS, METAMOKPHOSIS, AND THE FOSSIL RECORD PLATE 12 Jarmila Kukalova-Peck +C

- C + sc - sc -+R '-M +, cu

* IA + + - 2A - -

-

I 1 PLATE 13

EXPLANATION OF FIGURES

46 Major steps in pterygote evolution, sponsored by the development of juvenile wings: Pterygota were de- rived monophyletically from Apterygota through acquiring a paleopterous type of pro-wings on all nymphal body segments (A). In the paleopterous lineage, the meso/metathoracic wings in nymphs in- creased in size and became curved backwards (a),or flexed backwards (a') along the fold distal to the hinge line. In the neopteran lineage, which originated monophyletically from the early paleopteran stock by de- veloping a pivoting third axillary, the nymphal meso/metathoracic wings became streamlined by actively flexing backwards (b) along the fold within the hinge line. In both Paleoptera and Neoptera, the prothoracic and abdominal wings became more or less reduced. The endopterygote lineage probably origi- nated monophyletically from the juvenile plecopteroid Protorthoptera through the withdrawal of deemphasized wings (b') into suhcuticular pockets. Towards the Recent, in all (a, b, and b') lineages juvenile wings independently and parallelly decreased in size and/or became fused with the terga, and as a consequence developed a metamorphic instar. Evolution in adults (B):Outspread pro-wings in paleopterous ancestral pterygotes were flapping and were in elastic equilibrium for effortless soaring. In the paleop- teran-lineage, flapping forward flight occured first (c). In the neopteran lineage elastic equilibrium was lost due to wing flexing (d) and indirect flight musculature became involved in flight (d, d'). Towards the Recent, the wings often tended to become smaller and the wing beat frequency increased by auxilliary structures. Hypothetical early Pterygota: A. older nymph; B. adult. Examples of typical Paleozoic insects: a. Megasecoptera, nymph; b. Protorthoptera, nymph; c. Megasecoptera, adult; d. Protorthoptera, adult. Original. PLATE 12

ANCESTRAL U.PALEOZOIC RECENT PLATE 14

EXPLANATION OF FIGURES

47 Primitive neopteran nymph with wings occuring on three thoracic and ten abdom- inal segments (also fig. 35). Specimen 8592 ab, Museum of Camp. Zoology, Harvard Univ., Protorthoptera; total length 8 mm; Lower Permian, Kansas. Thoracic wings marked by three short arrows (wing outlines slightly retouched); abdominal wings, by a long arrow.

48 Fossil neopterous nymphal wing showing articulation to, not fusion with, the tergum, as opposed to the condition found in all modern nymphs. Free posterior wing margin is marked by two long arrows, free lateral margin of the tergum (showing through the superimposed wing), by a short arrow. Specimen 15789, fore wing. Peabody Museum, Yale Univ., Protorthoptera; wing length 8.7 mm; Lower Permian, Kansas .

124 INSECT WINGS, METAMORPHOSIS, AND THE FOSSIL RECORD PLATE 14 Jarmila Kukalova-Peck

125