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