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Episodes in Insect Evolution Timothy J 590 Episodes in insect evolution Timothy J. Bradley,1,* Adriana D. Briscoe,* Sea´n G. Brady†, Heidy L. Contreras,* Bryan N. Danforth,‡ Robert Dudley,§ David Grimaldi,ô Jon F. Harrison,k J. Alexander Kaiser,** Christine Merlin,†† Steven M. Reppert,†† John M. VandenBrooksk and Steve P. Yanoviak‡‡ *Department of Ecology and Evolutionary Biology, University of California Irvine, Irvine, CA 92697-2525, USA; †Department of Entomology and Laboratories of Analytical Biology, National Museum of the Smithsonian Institution, Washington, D.C. 20013-7012, USA; ‡Department of Entomology, Cornell University, Ithaca, NY 14853, USA; §Department of Integrative Biology, University of California Berkeley, Berkeley, CA 94720, USA; ôDivision of Invertebrate Zoology, Museum of Natural History, New York, NY 10024, USA; kSection of Organismal, Integrative and Systems Biology, School of Life Sciences, Arizona State University, Tempe AZ 85287-4501, USA; **Department of Basic Sciences, Midwestern University, Glendale, AZ 85308, USA; ††Department of Neurobiology, University of Massachusetts Medical School, Worcester, MA 01605, USA; ‡‡Department of Biology, University of Arkansas Little Rock, Little Rock, AR 72204, USA Synopsis This article derives from a society-wide symposium organized by Timothy Bradley and Adriana Briscoe and presented at the 2009 annual meeting of the Society for Integrative and Comparative Biology in Boston, Massachusetts. David Grimaldi provided the opening presentation in which he outlined the major evolutionary events in the formation and subsequent diversification of the insect clade. This presentation was followed by speakers who detailed the evolu- tionary history of specific physiological and/or behavioral traits that have caused insects to be both ecologically successful and fascinating as subjects for biological study. These include a review of the evolutionary history of the insects, the origins of flight, osmoregulation, the evolution of tracheal systems, the evolution of color vision, circadian clocks, and the evolution of eusociality. These topics, as covered by the speakers, provide an overview of the pattern and timing of evolutionary diversification and specialization in the group of animals we know as insects. Episodes in insect evolution flight (the origin of pterygote insects), complete Biologists often refer to the ‘‘success’’ of a group of metamorphosis (the origin of the Holometabola), organisms, which typically means one of two things: and eusociality (Grimaldi and Engel 2005). While evolutionary success—measured in terms of species the first three can be credited with the astonishing diversity, geological duration, and/or geographic diversity of millions of species of insects, the approx- spread—and ecological success, as measured in imately 17,000 species of eusocial insects are most terms of the impacts of a species or group of species significant in terms of their collective impact on upon an ecosystem. By either measure, insects are terrestrial environments (as well as their uniquely the most successful life form in the 450 million- complex societies). Each of these adaptive features year history of terrestrial living. They had appeared was a topic of discussion at the recent symposium at least by the early Devonian, and by the on insect evolution at the SICB meeting in Boston. Carboniferous some 80 million years later had When referring to ‘‘episodes’’ it must be cautioned evolved into a diverse array of winged forms. against thinking of these as sudden events. In fact, all Shortly thereafter they evolved metamorphosis, and complex adaptive features progress through stages it was not until the Late Jurassic or Early Cretaceous, of gradual modification taking millions to tens of 150–140 million years ago, that the first complex millions of years to refine. Wings and flight, for societies evolved. These ‘‘episodes’’ correspond to example, presumably evolved from lateral expansions what are probably the four major adaptive features of the insect body used for gliding, to fully of insects: terrestriality (the origin of hexapods), articulated structures capable of powered flight. From the symposium ‘‘Insect Evolution’’ presented at the annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2009, at Boston, Massachusetts. 1E-mail: [email protected] Integrative and Comparative Biology, volume 49, number 5, pp. 590–606 doi:10.1093/icb/icp043 Advanced Access publication June 24, 2009 ß The Author 2009. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: [email protected]. Insect evolution 591 Refinement of the pteralia or axillary sclerites at the most closely related to Crustacea (Giribet et al. base of the wing and of wing muscles then led to 2001; Hwang et al. 2001; Carapelli et al. 2005), and various abilities, such as folding the wings over the possibly they even are highly modified Crustacea back (neoptery), which then allowed for the invasion (Nardi et al. 2003; Giribet et al. 2005; Regier et al. of tight spaces while retaining the ability to fly (even 2005; Mallatt and Giribet 2006). Interestingly, within if just with the hind wings). Terrestrialization Crustacea are groups that some of the molecular required not only a waxy cuticle, but a tracheal respi- studies link to hexapods; these include species ratory system, an excretory system composed of that inhabit freshwater and alkaline lakes (like Malpighian tubules, as well as subsequent modifica- Branchiopoda), and so would seem to represent an tions of spiracular valves and cryptonephridia that ecological intermediate between fully marine crusta- reduced water loss. ceans and fully terrestrial insects. A crustacean origin Any consideration of terrestrialization in insects for hexapods has some morphological support, too. must address the origin of hexapods, which has This evidence includes, for example, gross brain been elusive. Traditionally, the living sister group structure (Nilsson and Osorio 1997; Whitington to Hexapoda has been thought to be the and Bacon, 1998), fine structure of the ventral Myriapoda (Snodgrass 1938; Boudreaux 1979; nerve cord (Whitington et al. 1996), and structure Hennig 1981; Kristensen 1991), based principally of the ommatidia, or facets, of the eye (Paulus 2000). on the loss of the second pair of antennae commonly Presumably, hexapods diverged from a common seen in Crustacea, and the presence of tracheal ancestor with Crustacea in the Silurian, more than respiratory systems in both of the terrestrial 420 million years ago. By the Early Devonian there is groups. There are other morphological features, definitive evidence in the Rhynie chert of Scotland though, that appear to link myriapods and hexapods: (ca. 410 myo) for Collembola (Hirst and Maulik loss of the mandibular palp (a structure that occurs 1926; Whalley and Jarzembowski 1981) and true in most Crustacea), presence of Malpighian tubules, Insecta (Engel and Grimaldi 2004). The well a tentorium (the internal, cuticular strut inside the preserved Devonian fossil Devonohexapodus bocksber- head capsule) bearing anterior arms, the presence of gensis, from the famous Hunsru¨ck Slate marine styli (pairs of small, nonsegmented, nonmusculated deposit of Germany, has been proposed as a stem- appendages on the coxae and/or abdominal ster- group hexapod (Haas et al. 2003). Intriguingly, nites), and of eversible vesicles (eversible, membra- this animal was reported to possess a single pair of nous structures similarly distributed), as well as antennae, a thorax with three long walking legs, the presence of a specialized sensory structure and an abdomen with numerous pairs of small, at the base of the antenna, the postantennal segmented ‘‘leglets,’’ nicely intermediate between (also called temporal, or To¨mo¨sva´ry) organ. hexapods and myriapods. This interpretation of Unfortunately, several of these characters are losses Devonohexapodus, however, has been criticized (mandibular palps, second pair of antennae), and (Willmann 2005), and as a result of the recent dis- absence of a structure is difficult to homologize. covery of a large series of well-preserved specimens, Based on the branching and fine structure of it is now known that Devonohexapodus is actually a tracheae, and on the positions and structure of synonym of Wingertschellicus from the same deposit spiracles, tracheae clearly evolved multiple times in (Briggs and Bartel 2001; Kuehl and Rust 2009). terrestrial arthropods, including the Hexapoda, The new material indicates that Wingertschellicus is Myriapoda, oniscoidean isopods, various arachnids, an enigmatic, ancient Crustacean with two pairs of and Onychophora (Ripper 1931; Dohle 1988; Hilken antennae, which is definitely not a hexapod. Thus, 1997; Kraus 1998). The postantennal organ may there is no known early stem-group hexapod, actually be homologous to the frontal organ although fossil evidence has been very clear about of Crustacea, and so may be a primitive feature of the origins of another major adaptive feature of hexapods. There is insufficient comparative work on insects: an aquatic lifestyle. arthropods’ Malpighian tubules to judge primary The basal pterygote orders Ephemeroptera and homology among the groups that possess them. Odonata have nymphs that live in fresh water, Thus, morphological support for a myriapodian and for this reason it is commonly assumed that origin of hexapods is essentially
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