Current Biology Magazine ABInsect evolution Michael S. Engel It goes without saying that insects 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. Animals from the early Ordovician Fezouata formations of Morocco. (A) The marrellomorph arthropod Furca (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 Hexapoda, the other being the Entognatha, 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 Diplura, Protura, and early Cambrian arthropod. Nature 490, 258–261. Collembola (springtails). While it is often Briggs, D.E.G. (2015). Extraordinary fossils 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 crustacean easy to recognize an insect and even a on Whittington (1975) ‘The enigmatic animal 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 fossil 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. Precambrian 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 R868 Current Biology 25, R845–R875, October 5, 2015 ©2015 Elsevier Ltd All rights reserved Current Biology Magazine 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 — Chelicerata, Crustacea, Myriapoda, and Hexapoda — the latter three united as the Mandibulata and set in opposition to the chelicerates, trilobites, and trilobite-like groups. Traditionally, Hexapoda were believed related to Myriapoda (centipedes, millipedes, 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 Remipedia as the living sister group to hexapods, or the more inclusive Xenocarida (Remipedia + the benthic Cephalocarida). 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 Metapterygota), 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 antenna, 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 ovipositor. 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 (Archaeognatha) and convergences between myriapods and Hexapoda, and fed on sporangia or silverfi sh (Zygentoma) 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 (Pterygota), 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 Dicondylia, 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