Current Biology Magazine

ABInsect evolution

Michael S. Engel

It goes without saying that epitomize diversity, and with over a million documented species they stand out as one of the most remarkable lineages in the 3.5-billion-year history of life on earth (Figure 1). This reality is passé to even the layperson and is taken for granted in the same way none of us think much of our breathing as we go about our day, and yet insects are just as vital to our existence. Insects 5 mm are simultaneously familiar and foreign to us, and while a small fraction are C beloved or reviled, most are simply ignored. These inexorable evolutionary overachievers outnumber us all, their segmented body plan is remarkably labile, they combine a capacity for high rates of speciation with low levels of natural extinction, and their history of successes eclipses those of the 10 cm more familiar ages of dinosaurs and mammals alike. It is their evolution — persisting over vast expanses of geological time and inextricably Figure 5. from the early Fezouata formations of Morocco. (A) The marrellomorph (Natural History Museum of Toulouse, France, MHNT. implicated in the diversifi cation of other PAL.2007.39.80.1). (B) A concretion preserving the giant fi lter feeding anomalocaridid Aegirocassis lineages — that stands as one of the benmoulai (Yale Peabody Museum YPM 237172). (C) Reconstruction of Aegirocassis benmoulai most expansive subjects in biology. © Marianne Collins. (Images reprinted by permission from Macmillan Publishers Ltd: Nature (Van Insects comprise the more diverse Roy et al., 2010 and 2015), copyright 2010 and 2015.) of two classes united together as the arthropod subphylum , the other being the , consisting FURTHER READING Ma, X., Hou, X., Edgecombe, G.D., and Strausfeld, N.J. (2012). Complex brain and optic lobes in an of the orders , , and early arthropod. Nature 490, 258–261. Collembola (). While it is often Briggs, D.E.G. (2015). Extraordinary reveal Rehm, E.J., Hannibal, R.L., Chaw, R.C., Vargas-Vila, the nature of Cambrian life: a commentary M.A., and Patel, N.H. (2009). The easy to recognize an and even a on Whittington (1975) ‘The enigmatic Parhyale hawaiensis: A new model for arthropod hexapod, identifying the closest relatives Opabinia regalis, Middle Cambrian, Burgess development. Cold Spring Harbor protocols of Hexapoda has been a pernicious Shale, British Columbia’. Phil. Trans. R. Soc. 2009(1):pdb.emo114. B 370, 20140313. Sansom, R.S., Gabbott, S.E., and Purnell, M.A.P. problem. Interestingly, while much has Cuthill, J.F.H., and Conway Morris, S. (2014). (2010). Non-random decay of chordate improved regarding arthropod phylogeny Fractal branching organizations of Ediacaran characters causes bias in interpretation. rangeomorph fronds reveal a lost Proterozoic Nature 463, 797–800. and the placement of hexapods, today body plan. Proc. Natl. Acad. Sci. USA 111, Seilacher, A. (1992). Vendobionta and we are somewhat less certain of a Psammocorallia: lost constructions of 13122–13126. evolution. J. Geological Soc. Lond. precise culprit for the hexapodan sister Erwin, D.H., Lafl amme, M., Tweedt, S.M., Sperling, 149, 607–613. E.A., Pisani, D., and Peterson, K.J. (2011). The group. This uncertainty highlights the Sperling, E.A., Frieder, C.A., Raman, A.V., Girguis, Cambrian conundrum: Early divergence and P.R., Levin, L.A., and Knoll, A.H. (2013). Oxygen, challenges in reconstructing relationships later ecological success in the early history of ecology, and the Cambrian radiation of animals. among major groups of Arthropoda and animals. Science 334, 1091–1097. Proc. Natl. Acad. Sci. USA 110, 13446–13451. Erwin, D.H., and Valentine, J.W. (2013). The Van Roy, P., Orr, P.J., Botting, J.P., Muir, L.A., Vinther, of interpreting broad patterns in the Cambrian explosion. (Greenwood Village, CO: J., Lefebvre, B., el Hariri, K., and Briggs, D.E.G. evolution of the phylum. Roberts). (2010). Ordovician faunas of Burgess Shale-type. Gaines, R.R., Hammarlund, E.U., Hou, X-.G., Qi, Nature 465, 215–218. C-.S., Gabbott, S.E., Zhao, Y-.L., Peng, J., and Van Roy, P., Daley, A.C., and Briggs, D.E.G. (2015). Hexapoda and the origin of insects Canfi eld, D.E. (2012). Mechanism for Burgess Anomalocaridid trunk limb homology revealed Relationships among Arthropoda have Shale-type preservation. Proc. Natl. Acad. Sci. by a giant fi lter-feeder with paired fl aps. Nature USA 109, 5180–5184. 522, 77–80. long been a matter of debate, and Gould S.J. (1989). Wonderful life. The Burgess even monophyly of the phylum was Shale and the nature of history. New York: Department of Geology and Geophysics and once called into question. The door to W.W. Norton and Company. Yale Peabody Museum of Natural History, Lafl amme, M. (2014). Modeling morphological arthropod polyphyly has been closed, diversity in the oldest large multicellular Yale University, PO Box 208109, New Haven, organisms. Proc. Natl. Acad. Sci. USA 111, CT 06511, USA. however, and with the recognition of 12962–12963. E-mail: [email protected] the relationship of Cycloneuralia to

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the panarthropod phyla (Arthropoda, Tardigrada, Onychophora), much of what we understand about arthropod evolution has been transformed. The quixotic Cambrian Rhinochelata (Opabiniida) and Radiodonta (Anomalocarida), diverging from a grade of basal lobopods (see the Quick guide in this issue), were stem groups to the Euarthropoda and its more familiar extant lineages — , Crustacea, , and Hexapoda — the latter three united as the and set in opposition to the chelicerates, trilobites, and trilobite-like groups. Traditionally, Hexapoda were believed related to Myriapoda (, , and their kin), united by the presence of tracheae, or a network of exoskeletal invaginations for the transport of air and related to their shared terrestrial life. Current evidence refutes this association and considers the tracheates as independent groups at opposing ends of the mandibulate spectrum, with hexapods nested in a paraphyletic Crustacea. Many studies implicate the small, blind, and anchialine cave- inhabiting as the living sister group to hexapods, or the more inclusive Xenocarida (Remipedia + the benthic ). Morphological support for the Anartiopoda (xenocarids + hexapods) is scant, although at least Figure 1. Nature’s inordinate fondness for six legs. among the cephalocarids the reduced Modern hexapod diversity representing the summation of over 400 million years of high speciation number of segments and loss of rates and low levels of natural extinction (©Grimaldi and Engel, Evolution of the Insects, Cambridge abdominal appendages is somewhat University Press). hexapod-like. While Tracheata are considered defunct, support remains putatively closer to insects owing to the abdominal segment (secondarily lost for such a grouping, particularly in the presence of cerci, paired claws, and a in ), the presence of a arrangement of pleural sclerites, the similar gonopore position. However, all chordotonal organ and loss of intrinsic remnants of the subcoxa which are of these traits are likely plesiomorphic musculature in the , the loss homologous to the crustacean coxa. The (primitive), particularly if the caudal rami of articulations between the thoracic Xenocarida + Tracheata is tantalizing as of xenocarids are homologous to cerci. sterna and coxae, and the presence xenocarids resemble what one would Regardless of entognathan monophyly, of an . Primitive insects were expect of a marine stem-tracheate, the fi rst insects were fully terrestrial, wingless, and the apterous orders obviating the need to explain apparent as was the common ancestor of of bristletails () and convergences between myriapods and Hexapoda, and fed on sporangia or silverfi sh () give us our hexapods. Tragically, fossils of stem- scavenged. closest concept of what the original group hexapods remain elusive. Considerable effort has been insect might have resembled. These Despite the challenges of identifying expended to resolve relationships orders form a grade leading to the their nearest relatives, hexapod among insects, focusing almost winged insects (), with monophyly is strongly supported by exclusively on the modern diversity. Zygentoma sharing with pterygotes diverse data sources. Noteworthy Although there are numerous particulars important features in the mandible morphological features include the that are debated, some broad patterns and ovipositor. Of particular interest is reduction of abdominal segments are consistent across sources of data their shared dicondylic mandible, with and appendages, legs composed and methods of analysis. No serious its two points of articulation, which of six podites, and, of course, the challenge has ever been mounted imposes unidirectional movement and three appendage-bearing thoracic to insectan monophyly. Among permits greater force. The signifi cance segments, from which is derived their the more notable of morphological of this grouping, the , cannot name. Recognition of Entognatha is characters supporting Insecta are the be underestimated as it is of paramount sometimes contested, with Diplura medial caudal fi lament of the eleventh importance for understanding one of

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the most signifi cant events in Animal dragonfl ies, and damselfl ies (both of varied developmental patterns, but evolution — the origin of fl ight. ). Subsequent modifi cations shares morphological resemblance permitted fl exion of the wings over the across all stages, nymphs effectively Insects take to the skies abdomen and gave rise to the . being miniaturized adults with wing Pterygota, the winged insects, are This seemingly simple act is the result buds. Fully-functional wings and sexual indisputably monophyletic, representing of a complex arrangement of minute maturity appear in the adult at which a single origin of wings and fl ight among sclerites at the base of the wing, and point molting ceases. Mayfl ies have a insects. In a world where our attention the action of muscles attached to transitional form whereby wings become is snared by charismatic birds, bats, one in particular — the third axillary, a functional one molt prior to the adult — or long-lost pterosaurs, it is easily characteristically Y-shaped plate that the subimago. This subimaginal molt overlooked that insects were the fi rst when moved collapses the posterior is homologous to the post-adulthood animals to evolve fl ight and dominated portions of the wing like an accordion. molts of ametabolous insects, and the the planet’s skies up to 170 million years Flexion permits neopterans to invade loss of this stage is a dramatic feature before any contenders. Flight is ancient tight spaces without damage to their of Metapterygota. From an evolutionary and insects took to the air not long after wings, and also paves the road for perspective, the appears to invaded land, with pterygote specializations unrelated to fl ight. represent a protracted hemimetabolan remains dating back 410 million years. The Neoptera are organized into two pronymph. The pronymph is a brief, With such dramatic diversity among principle lineages, the often-unnoticed stage between hatching insects, it is no wonder that the wings and the ( + and the fi rst nymphal instar, and themselves have been modifi ed into any Holometabola). Polyneoptera are a pronymphs sometimes never depart number of forms, frequently associated heterogeneous assemblage of orders the egg. Pronymphs share anatomical, with the specifi c mechanics of fl ight and covers the (Dermaptera), physiological, and embryological features involved, or have been coopted for crickets, katydids, and with larvae, and prolongation of this purposes other than fl ying —defense (), stick and leaf insects stage provides greater control over (inclusive of crypsis), communication, (), stonefl ies (), development. The pupa is conversely mating, or thermoregulation. webspinners (Embiodea), zorapterans a compaction of the various nymphal It is between the silverfi sh-like (), crawlers (), stages prior to eclosion as an adult. common ancestor of Dicondylia and (Mantodea), roaches (Blattaria), The Holometabola comprises nearly Pterygota that the fi rst fl yer appeared. and (Isoptera). The Paraneoptera 85% of insect diversity and today While the functional morphology of the includes the barklice (), true contains more species than there is robustly understood, the lice (Phthiraptera), (Thysanoptera), are among plants or all other animal more abominable mystery has been the and the prominent plant-feeding true phyla combined (Figure 1). Orders origin of the structure itself. Whereas bugs (). While one should include the , , and other the vertebrate wing is invariably a never disparage the variety resident (), lacewings and modifi ed forelimb, the air foil of insects among Polyneoptera and Paraneoptera, (), dobsonfl ies and is of other derivation and pterygotes when truly speaking of insect diversity alderfl ies (), snakefl ies retain the full complement of six legs. it is in reference to Holometabola. (Raphidioptera), twisted-wing Hypotheses for the origin of the insectan Holometabola include those orders with parasitoids (), wing are as diverse as the organisms complete , an innovation (Coleoptera), scorpionfl ies (), themselves, most based on elaborate that, like fl ight, was crucial for insectan nannochoristids (Nannomecoptera), adaptive or functional scenarios hegemony. snow fl eas (Neomecoptera), true fl eas divorced from phylogenetic reasoning. (Siphonaptera), true fl ies (Diptera), Presently, phylogenetic, morphological, A developmental shift caddisfl ies (Trichoptera), and paleontological, developmental, and Holometaboly, or complete and butterfl ies (). The genetic evidence indicates that the wing metamorphosis, is typifi ed by a soft- advent of the larva did not immediately is a planar extension of the back of the bodied, morphologically-reduced larva, confer tremendous advantages that exoskeleton. The genetic architecture followed by a largely quiescent pupa. led to a proliferation of species, as for a moveable joint already existed for The larva often has a diet and life quite holometabolans were spectacularly the leg and this machinery was coopted independent from that of the adult, meager for epochs after their emergence. and amalgamated to regulate formation permitting a single species to effectively Moreover, it seems heretical but of a hinge at the wing base. Flight fi rst live divergent existences. Larvae often Holometabola per se are not diverse, as evolved to access food and aid dispersal occur in protected habitats and can it is only from among apocritan wasps, in a world in which oxygen levels were enter prolonged periods of diapause staphylinoid and phytophagan beetles, rising and as vascular plants were during times of stress. Archaeognatha higher fl ies, and ditrysian moths that the making inroads into otherwise barren and Zygentoma have virtually no species-rich Behemoths emerge. landscapes. Insects gave the world fl ight, change in appearance from nymph to Each of these were independent and fl ight gave them the world. the sexually mature adult, owing to the triumphs achieved at different times. Early-diverging lineages of Pterygota absence of wing buds (ametaboly), There was no explosive holometabolan had wings with fi xed, outstretched and molting occurs throughout or ‘’ radiation, and we concatenate positions, their only extant descendants life. Hemimetaboly, or incomplete into single episodes eons of shifting being today’s mayfl ies (Ephemeroptera), metamorphosis, encompasses a range climates, changing geography, and

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simple chance, speaking of evolutionary A radiations as though they took place in ecological space and time and as adaptive responses. Yet, ecological interactions operate quickly, sometimes within dozens of generations, and lose their impact when attempting to explain patterns covering tens of millions of years. Nonetheless, the appearance B C of a larva permitted any number of subsequent evolutionary innovations key to their prosperity, such as endoparasitism.

A long history Fossils provide the only direct evidence we have of ancient life, permitting one to understand the proper paleogeographical, paleoclimatological, and paleoecological context for the DE origins of biological phenomena. The fossil record of insects is far more extensive than most individuals, including many entomologists, would assume (Figure 2). The earliest evidence of hexapods and true insects is in the Early chert of Rhynie, Scotland (411 million years ago). This fauna preserves a remarkably modern , praecursor, and a true insect, hirsti. A third species, Figure 2. Insects through the ages. Leverhulmia mariae, originally described (A) The largest insect ever, Meganeuropsis permiana (Protodonata), and Early griffenfl y from as a myriapod, has been reinterpreted the of central Kansas, USA. (B) A giant, stem-group fl ea, Pseudopulex wangi as a bristletail. Although fragmentary, (Protosiphonaptera), that fed on feathered dinosaurs or early Avialae in the middle of Inner Mongolia. (C) The earliest microphysid bug, Popovophysa entzmingeri (Hemiptera), in Canadian Late R. hirsti is signifi cant as it has traits amber. (D) A solitary , Oligochlora eickworti (Hymenoptera), in Early Miocene amber known only among winged insects, from the . (E) Perhaps the most spectacular fossil butterfl y known, the nymphaline revealing the early origin for fl ight. From Prodryas persephone (Lepidoptera), from the Eocene-Oligocene boundary of Florissant, Colorado, these few species it is apparent that USA. (Panels A and E, ©President and Fellows of Harvard College, Museum of Comparative Zoology, hexapods had diversifi ed suffi ciently Harvard University; B, reproduced with permission from Diying Huang; C, courtesy of R.C. McKellar; © such that derived entognaths, apterous D, Grimaldi and Engel, Evolution of the Insects, Cambridge University Press). insects, and even early pterygotes were present. Furthermore, they reveal The epochs following the hexapod some ponderous Paleozoic pterygotes that insects must extend into the gap were dominated by stem-group bearing wingspans between 500 and 710 and alongside those arthropod Ephemeroptera and Odonata, as well millimeters, but the majority of species lineages transitioning to land at that time as the fi rst major lineage of specialized remained at proportions comparable (myriapods, chelicerates). herbivores, the Palaeodicyopterida. to today. The earliest holometabolans Unfortunately, there is a lengthy gap Palaeodictyopterida were a group appeared in the Late , all in the hexapod record and spanning a of orders that proliferated during the minute and as scarcely-recognizable 65-million-year window from 385–325 Paleozoic, experiencing peak diversity stem groups, but by the Permian more million years ago. Prior to the ‘hexapod in the Late Carboniferous, and whose familiar-looking species make their debut, gap’ we know that insects had already mouthparts were modifi ed into a including primitive beetles, lacewings, diversifi ed suffi ciently to give rise to piercing beak used to feed on plant and varied mecopteroid-like relatives of Pterygota, while immediately after a fl uids, although whether some were Antliophora and . broad spectrum of supraordinal lineages predatory cannot be excluded. These The End Permian Event (252 million is established. It is therefore within species occurred during a period of years ago) closed the Paleozoic with the the hexapod gap that the majority of hyperoxia, permitting more effective most punishing mass extinction in earth insectan diversifi cation took place, oxygen transport via tracheae to the history, and the only one to have altered complete with the origins of Neoptera metabolically-active fl ight muscles. insect diversity at ordinal levels, removing and at least Polyneoptera and stem- Increased oxygen levels permitted and from the fauna the Palaeodictyopterida group Eumetabola. contributed to insect gigantism, with and stem-group orders to the

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paleopterous and polyneopterous permitted subsets of the social insect natural levels of extinction. This has insects. This removal of dominant lineages to dominate over their more been brought about through often high players gave opportunity to those who primitive forbearers, in what has been reproductive capacity, brief average survived to become the preeminent dubbed by Hölldobler and Wilson as generation time, large effective population faunal elements, and it is in the “dynastic succession”. size, and an amalgamation of traits that that the insect fauna becomes more The appearance of fl owering plants work synergistically. These are: fi rst, familiar, at least at higher levels, and early in the Cretaceous and their considerable developmental fl exibility due numerous clades made signifi cant rapid rise to fl oristic dominance by to redundant metameric components; forays into freshwater ecosystems. Early the closing stages of the Mesozoic second, a resilient arthropod exoskeleton species belonging to the crown group of radically altered the biotic landscape. and protective tracheal system many orders make their debut across the Any number of plant-associated engendering a large surface area to Triassic and Jurassic, including earwigs, insects were impacted by this shift volume ratio; third, fl ight, and more true roaches, mantises, termites, wasps, and those new resources offered by importantly neopterous wings to protect true fl ies, and moths, among others. angiosperms. Changing fl oras meant their primary means of dispersion, prevent The origin and various waves of those connoisseurs of host plants then wings from hindering entrance into diversifi cation of ecologically ubiquitous dwindling in diversity and abundance tight spaces, and allow their cooption groups occurred during the latter half faced extinction, while generalists or for other purposes; and fourth, a larva of the Mesozoic. Social groups such as newly emerging angiosperm specialists simultaneously permitting accelerated the termites, ants, and select groups found an increasingly prevalent resource. development, potential for protracted of eusocial bees appear during this Flowering plants were a necessity for diapause, and separation of immature time, the earliest societies being those the ascendancy of groups such as bees, and adult diets and modes of life. of the termites, although each took leaf beetles, , and moths, but it is When such a powerful combination tens of millions of years to achieve naïve to believe that this alone explains of factors is permitted to run over predominance. The hyperdiverse their boom. Angiosperms provided a new hundreds of millions of years, the natural weevils and chrysomeloid beetles also ‘landscape’ for initial allopatric speciation byproduct is unrivaled diversity. The arose during the Jurassic, as did the in such groups, but it was continued resilience of insects to major extinction infamous fl eas, originally ectoparasites cladogenesis fueled by subsequent events attests to the potency of low of feathered dinosaurs and subsequently biotic and abiotic events from which their volatility, although humankind’s artifi cial specialized for mammals and birds. It is hefty numbers were accumulated. The elevation of extinction rates and during the latest Jurassic that the fi rst full story of success for each spans over concurrent depression of speciation insect societies arose. Termites were the 165 million years and involves global potential through degraded habitat fi rst hexapods to evolve such behavior, events as dramatic as rifting continents, homogenization is a lethal concoction. a system facilitated by the collective fl uctuating climates, and extraterrestrial Insects are better prepared to contend construction of a nest. Eusocial behavior, impacts, as well as the world’s with an asteroid impact. whereby individuals live cooperatively blossoming. The tale of insect evolution to raise a common brood but in which is lengthy and we should not relegate it FURTHER READING the majority of individuals of the worker to titillating soundbites. Beutel, R.G., Friedrich, F., Yang, X.-K., and Ge, S.-Q. caste forego their own reproduction The Cretaceous–Tertiary mass (2013). and Phylogeny (Berlin, in place of that of the queen’s. In the extinction that so characteristically Germany: Walter de Gruyter). Engel, M.S., and Grimaldi, D.A. (2004). New light shed Early and mid-Cretaceous the termites ushered out of this world the non-avian on the oldest insect. Nature 427, 627–630. would be followed by analogous social dinosaurs had a comparatively negligible Engel, M.S., Davis, S.R., and Prokop, J. (2013). Insect wings: The evolutionary development of Nature’s systems appearing in the ants and impact on insects at higher levels. The fi rst fl yers. In Arthropod Biology and Evolution, select groups of stinging wasps and subsequent Cenozoic experienced A. Minelli, G. Boxshall, and G. Fusco, eds. bees. Interestingly, although sociality is a swings in global climate, from the (Berlin, Germany: Springer Verlag). pp. 269–298. Grimaldi, D.A. (2010). 400 million years on six legs: remarkable phenomenon, this complex Paleocene-Eocene Thermal Maximum On the origin and early evolution of Hexapoda. of behavioral repertoires, morphological (56 million years ago), with its massive Arthropod Struc. Dev. 39, 191–203. Grimaldi, D., and Engel, M.S. (2005). Evolution of the specializations, and physiological outpouring of carbon and global warming Insects (Cambridge, UK: Cambridge University alterations did not lead to immediate run amuck, to the later dramatic cooling Press). success or dominance for their of the Eocene–Oligocene Transition (34 Lieberman, B.S., and Melott, A.L. (2013). Declining volatility, a general property of disparate systems: respective groups. Indeed, in each case million years ago). Climate is one of the from fossils, to stocks, to the stars. Palaeontology these insects were social, sometimes best predictors of insect distributions and 56, 1297–1304. Nel, A., Roques, P., Nel, P., Prokin, A.A., Bourgoin, in clearly complex societies, but did not activity, and it is no surprise that these T., Prokop, J., Szwedo, J., Azar, D., Desutter- achieve the ecological abundance we events wielded signifi cant infl uence, Grandcolas, L., Wappler, T., et al. (2013). The typically associate with sociality until particularly the southward contraction of earliest known holometabolous insects. Nature 503, 257–261. tens of millions of years later. Sociality once widespread lineages as the planet Truman, J.W., and Riddiford, L.W. (1999). The origins of may have well poised select insect cooled and dried. insect metamorphosis. Nature 401, 447–452. clades, but it alone did not bestow upon its bearers hegemony. Instead, the Explaining success Division of , Natural History Museum, and Department of Ecology & eventual appearance of large, perennial Insect success can be summed up by Evolutionary Biology, University of Kansas, colonies coupled with further ethological, the low volatility anomaly, the result of Lawrence, KS 66045-4415, USA. anatomical, and chemical specializations high speciation rates coupled with low E-mail: [email protected]

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