CY501-C09[331-356].qxd 2/15/05 11:14 AM Page 331 quark11 27B:CY501:Chapters:Chapter-09: 9 TheThe Holometabola Holometabola Holometabola are those insects with so-called complete The holometabolous lineages account for the stunning metamorphosis, versus insects that are hemimetabolous diversity of insects, since Holometabola comprise nearly 85% (incomplete metamorphosis), or (as in the case of aptery- of all insects, and in this regard the feature is usually considered gotes) insects that display virtually no changes from imma- one of the two most important innovations of insects along ture stages to adult (ametabolous). Metamorphosis itself with wings. There is no doubt that Holometabola is a mono- refers to a dramatic change in an organism from one devel- phyletic lineage (e.g., Kristensen, 1975, 1999a; Hennig, 1981; opmental stage to another, which occurs in some amphib- Whiting et al., 1997; Whiting, 2002), though a similar “pupal” ians and various invertebrates, including many marine and stage has evolved independently in whiteflies (Aleyrodoidea: terrestrial arthropods. In hemimetabolous insects, which Sternorrhyncha) and thrips (Thysanoptera), wherein late instar include the paleopterans, polyneopterans, and paraneopter- nymphs are reduced, nonfeeding, and quiescent. These are ans, which are groups we have already discussed in detail, the entirely convergent with holometabolan pupae, though, based wing buds increase in size with each nymphal instar (e.g., on relationships and the fact that these paraneopterans do not Figure 9.1). Holometabolous insects have a soft-bodied, wing- have a larval stage. The most recent and comprehensive pres- less, morphologically reduced larval stage and a mostly qui- entation of insect development is the comprehensive treat- escent pupal stage. Adults of all insects are defined as those ment by Heming (2002). As we discuss later, the adaptive individuals that are reproductively mature, even in species advantage of the insect larva is not entirely clear, and larvae where the mature female is larviform or paedogenic, retain- may in fact provide multiple improvements over nymphal ing some or most larval features. Examples of paedogenic development. female holometabolans include most Strepsiptera (Fig- ure 10.80), some Diptera (e.g., Miastor [Cecidomyiidae]), and some Coleoptera (e.g., Micromalthus, a few Ripiphoridae), PROBLEMATIC FOSSIL ORDERS among others. The larva is the truly defining feature of Holometabola. Two extinct “orders” are enigmatic and have uncertain posi- This immature form is generally a slender, soft-bodied insect tion, though these have generally been affiliated with the with three short pairs of thoracic legs or none (sometimes Holometabola. The Paleozoic Miomoptera have been consid- they also have abdominal prolegs), and no external wing ered to be stem-group Holometabola even though their buds. Primitively they have a sclerotized head capsule with venation could also be interpreted as primitive relative to mandibles, minute palps and antennae, and reduced eyes or Paraneoptera. The other order, the Glosselytrodea from the usually just isolated ommatidia separated into stemmata. Paleozoic and Early Mesozoic, is perhaps a composite group, During metamorphosis, which takes place as a pupa, much apparently consisting of stem-group Neuropterida and fami- or all of the larval cuticle is replaced with adult cuticle. This lies of uncertain phylogenetic affinity. new cuticle derives from imaginal discs (sometimes also called by the German term, anlage), including the legs, eyes, MIOMOPTERA genitalia, and wings. Imaginal discs are pockets of specialized larval epidermal cells (histoblasts) that lie under the cuticle; The Miomoptera were generally minute insects, with fore- the histoblasts proliferate and differentiate during the late and hind wings similar in shape and venation (Figure 9.2). larval and pupal stages. An internal development of wings is The hind wings lacked an anal lobe, and both sets of wings why Holometabola are also sometimes called Endopterygota lacked crossveins. Little is understood of miomopterans (e.g., Kristensen, 1999a). because they are known almost entirely as wing fragments. 331 CY501-C09[331-356].qxd 2/15/05 11:14 AM Page 332 quark11 27B:CY501:Chapters:Chapter-09: 332 EVOLUTION OF THE INSECTS 9.1. Nymphal stages and the adult of a typical hemimetabolous insect, a barklouse (Psocoptera: family Lepi- dopsocidae). Holometabolan metamorphosis involves larval and pupal stages. Scanning electron micrographs. Where body fragments are known, species were apparently the Metropatoridae are presently unknown from the Per- mandibulate and had conspicuously thick antennae, with mian, while the other two families are also known from the 15–20 antennomeres; tarsi were four-segmented; and the Permian. cerci were short. The position of Miomoptera is extremely unclear but they have been treated by most authors as stem- GLOSSELYTRODEA group Holometabola (e.g., Rasnitsyn and Quicke, 2002). They have even at times been considered as a stem group to The glosselytrodeans as presently constituted (Carpenter, the Hymenoptera (e.g., Rasnitsyn, 1980). Martynov (1938) 1992) may be an unnatural group, consisting on the one originally asserted that Miomoptera were allied to the Ple- hand of the Early Permian Permoberothidae and on the coptera, but, like the Holometabola hypothesis, there is lit- other hand as an assemblage of Late Permian and Triassic- tle evidence to support this notion. Miomoptera are herein Jurassic families (Archoglossopteridae, Glosselytridae, Glos- considered as stem-group Paraneoptera (Figure 4.24) but sopteridae, Jurinidae, Polycytellidae, and Uskatelytridae). may eventually be considered allies of the Psocodea or The Permoberothidae are stem-group Neuropterida (e.g., Condylognatha. Carpenter, 1943a). Permoberothidae should perhaps be There are presently only three families included in referred to as Protoneuroptera (Figure 9.2), and the Glosse- Miomoptera. Various authors have placed several other fam- lytrodea should be restricted to the aforementioned suite of ilies in the order, but many of these had large anal fans in the families. The straight CuP vein marking off a distinct anal hind wing and numerous crossveins and appear to be more region with crowded anal veins and the relatively straight MA polyneopterous in character. The polyneopterous families vein running beside the anterior of MP is reminiscent of included by earlier authors have all been removed to the some Jurinidae, which was the justification for unifying Per- “Protorthoptera” or to Neoptera incertae sedis. The order is moberothidae with other Glosselytrodea. The tegminous known only from the Late Carboniferous and Permian, hav- forewings of Glosselytrodea s.str. have a superficial resem- ing apparently gone extinct during the End Permian Event. blance with protocoleopteran elytra, perhaps also furthering All three families are known from the Late Carboniferous but the notion that these families were “neuropteroid.” CY501-C09[331-356].qxd 2/15/05 11:14 AM Page 333 quark11 27B:CY501:Chapters:Chapter-09: THE HOLOMETABOLA 333 Glosselytrodea s.str. are relatives of the Orthoptera. The phylogenetic position of glosselytrodeans remains con- tentious, and considerable work remains to be undertaken before Glosselytrodea s.str. can be considered to be clearly polyneopterans. THE ORIGINS OF COMPLETE METAMORPHOSIS Given the great success of holometabolans, the major question is: How did they evolve? Just like wings and any other feature of adaptive significance, there is a spectrum of specialization in holometaboly, perhaps the most important aspect involving the imaginal discs. In the more basal holometabolans, such as neuropterids, many beetles, mecopterans, nematocerous flies, and symphytan wasps, some of the larval epidermis is retained in the adult. Imaginal discs in these groups develop in the last larval instar. In cyclorrhaphan Diptera, Lepi- doptera, and apocritan Hymenoptera, all or virtually all of the adult cuticle is formed from imaginal discs, and the imaginal discs begin developing in the embryo, which is a more evolved form of holometaboly. Most of the work on imaginal discs has been done on Drosophila melanogaster since disc development can be manipulated not just experimentally but genetically as well. This fly has a series of imaginal disc pairs that develop into the adult head (the labial, humeral, clypeolabral, and antennal-eye discs), the thorax (the fore-, 9.2. Wings of the problematic orders Miomoptera and “Glosse- mid, and hind legs, wing, and halter discs), and abdomen lytrodea,” which may have had close affinities to the Holometabola. From top to bottom, Eodelopterum priscum (Archaemiopteridae) from (the genitalic discs and four small groups of histoblasts) (Fig- the Late Carboniferous of Germany, Jurina marginata (Jurinidae) from ure 9.3). In the case of appendages, as these develop they the Permian of Central Asia, and Permoberotha villosa (Permoberoth- idae) from the Early Permian of Kansas. expand and either fold on itself or telescope to fit within the confines of the imaginal disc pocket; they then unfold and expand upon pupation and further upon eclosion. Each disc The Glosselytrodea s.str. had very distinctive wings (Fig- has compartments of predetermined regions that develop ure 9.2). Most were relatively small insects, with wings sub- into particular structures. The extensive work on Drosophila equal in shape and size. The forewing possessed an expanded has revealed