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Phylogeny and Evolution of Neuropterida: Where Have Wings of Lace Taken Us?

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Phylogeny and Evolution of Neuropterida: Where Have Wings of Lace Taken Us? EN63CH27_Engel ARI 20 November 2017 14:5 Annual Review of Entomology Phylogeny and Evolution of Neuropterida: Where Have Wings of Lace Taken Us? Michael S. Engel,1,2 Shaun L. Winterton,3 and Laura C.V. Breitkreuz1,2 1Division of Entomology, Natural History Museum, Lawrence, Kansas 66045-4415, USA; email: [email protected], [email protected] 2Department of Ecology and Evolutionary History, University of Kansas, Lawrence, Kansas 66045-4415, USA 3California State Collection of Arthropods, California Department of Food and Agriculture, Sacramento, California 95832-1448, USA; email: [email protected] Annu. Rev. Entomol. 2018. 63:531–51 Keywords The Annual Review of Entomology is online at lacewings, Megaloptera, phylogeny, Raphidioptera, systematics ento.annualreviews.org https://doi.org/10.1146/annurev-ento-020117- Abstract 043127 Annu. Rev. Entomol. 2018.63:531-551. Downloaded from www.annualreviews.org The last 25 years of phylogenetic investigation into the three orders con- Copyright c 2018 by Annual Reviews. stituting the superorder Neuropterida—Raphidioptera, Megaloptera, and All rights reserved Access provided by Texas A&M University - College Station on 01/28/18. For personal use only. Neuroptera—have brought about a dramatic revision in our understanding of the evolution of lacewings, snakeflies, dobsonflies, and their diverse rela- tives. Phylogenetic estimations based on combined analyses of diverse data ANNUAL REVIEWS Further sources, ranging from adult and larval morphology to full mitochondrial Click here to view this article's genomic DNA, have begun to converge on similar patterns, many times in online features: • Download figures as PPT slides accordance with hypotheses put forth by Cyril Withycombe nearly a cen- • Navigate linked references • Download citations tury ago. These data, in combination with information from the fossil record, • Explore related articles • Search keywords have given a revised perspective on the historical evolution and classifica- tion of Neuropterida, necessitating an overhaul of their organization and providing focus and insight on fruitful future efforts for neuropterology. 531 EN63CH27_Engel ARI 20 November 2017 14:5 INTRODUCTION Holometabolous insects are the paragons of biodiversity, with their numbers of species and indi- Gula: a sclerite viduals dominating terrestrial ecosystems (34). The bulk of this species richness belongs to clades located ventrally on within the four megadiverse groups—Coleoptera, Lepidoptera, Hymenoptera, and Diptera— the head capsule of with the remaining lineages relegated to so-called minor orders. Neuropterida are one such lin- some prognathous eage, though when considering their evolutionary history, they could never be considered minor. insects, posterior to the submentum Whether as a single order or under the current tripartite scheme, Neuroptera, Megaloptera, and (labium) and usually Raphidioptera are among the most recognizable and charismatic insects, encompassing the snake- between the postgenae flies, alderflies, dobsonflies, dustywings, antlions, and familiar lacewings among their many other Stem group: relatives (Figure 1). a paraphyletic Here, we summarize the current consensus on relationships among the main lineages of Neu- assemblage, excluding ropterida, with brief synopses of their evolution, diversity, and biology. Current syntheses of the crown group; it is molecular and morphological data are converging on relationships that harken back to Cyril sufficient to denote such taxa as Withycombe (1898–1926) (123). Thus, a recurrent theme in modern neuropterology is that stem-group X, rather many historical schemes are supported by our contemporary science. This does not imply a than proliferate need for a retrograde reclassification of Neuroptera but instead a renewed appreciation of our uninformative, minute intellectual forebears. In addition, we have attempted to provide some foils against which future taxa of identical research might joust, in the hopes of stirring new advances in our understanding of lacewing categorical rank to their associated crown evolution. group or mislead by regarding a paraphyletic taxon to be the sister to the MONOPHYLY AND RELATIONSHIPS AMONG crown group NEUROPTERID ORDERS Crown group: The monophyly of Neuropterida has not been a matter of serious debate, and every robust, modern a monophyletic, more attempt at estimating relationships among the principal lineages of Holometabola has recovered recently evolved the clade (70, 110) and supported it as sister to Coleoptera or Coleoptera + Strepsiptera (70, 89, lineage 101, 102, 110). Opinion about the relationships among the three orders, by contrast, has gone back and forth over recent decades, converging upon a Megaloptera + Neuroptera clade (Eidoneu- roptera) relative to Raphidioptera (111, 120). The alternative of Raphidioptera + Megaloptera was argued for owing to shared telotrophic ovarioles, grooming behavior, specializations of the tho- rax, and a gula (46, 47); however, these are inconsistent in light of current phylogenetic estimates and the homology of those varied sclerites lumped as gulae in distant taxa, and the polarity and distribution of telotrophic ovarioles are suspect (20, 38). For now, the Eidoneuroptera hypothesis is the one most widely supported by diverse sources of data (18, 111, 120, 126). Annu. Rev. Entomol. 2018.63:531-551. Downloaded from www.annualreviews.org The Neuropterida as a whole are today largely relict but not primitive. In fact, most lineages of Holometabola diverged early in the Carboniferous or latest Devonian (70, 73, 110), with the Access provided by Texas A&M University - College Station on 01/28/18. For personal use only. ancestral lineage of Neuropterida + Coleopterida emerging after divergence from the lineages leading to Panorpida and Hymenopterida (110). Records and calibrated estimations are for stem groups, whereas taxa that we might ascribe to crown-group Neuropterida are not known until the Early Permian and most extant families not known until the Mesozoic (Figure 2), much as is true for other holometabolan lineages (34). Two extinct groups from the Early to Late Per- mian, Permoberothidae and Permithonidae (Protoneuroptera), are most likely representatives of earlier stem-group eidoneuropterans (34, 90). The group is heterogeneous, however, and some permithonids may be more closely related to Neuroptera. Some of these species had been impli- cated as stem-Megaloptera but lack any shared features with Megaloptera (90). Modern genera and species are nonetheless relict in that the phylogenetic diversity, biological and morphological disparity, and breadth of distribution across the clade have decreased over geological time. 532 Engel · Winterton · Breitkreuz EN63CH27_Engel ARI 20 November 2017 14:5 ab cd e e a a d i d e i i NNemopteridae l a SSisyridae d l i d e i e i e s l m h a AAscalaphidae c y a d p o i p s r o d l e c i a n y a d p IInocellidae i a RRaphidiidae r t SSialidae la a o e NNymphidae p e CCorydalidae e y r a e h i m d id a id r d p a i a a h e l n i e i o d DDilaridae a th ae e IIthonidae d pi tis an o MMantispidae e f da psi cho PPsychopsidaesy CChrysopidaehry sopidae MMyrmeleontidae yrm ele ont idae n ae g id th RRhachiberothidae ro e h e CConiopterygidae BBerothidae a a id o c i n h b e a i i o o b r d e i p e e r m h t o t a e e r t HHemerobiidae d r h o i y r l i g d v y m i a h e d m e NNevrorthidae s a e OOsmylidae Annu. Rev. Entomol. 2018.63:531-551. Downloaded from www.annualreviews.org Access provided by Texas A&M University - College Station on 01/28/18. For personal use only. l k j i Figure 1 Extant diversity of Neuropterida. Representative species clockwise from upper left, with families of Neuroptera in shades of green and offset portions encompassing Raphidioptera (shades of orange) and Megaloptera (shades of blue): (a) Eremoides bicristatus (Ascalaphidae), (b) Chasmoptera hutti (Nemopteridae), (c) Agulla sp. (Raphidiidae), (d ) Archichauliodes sp. (Corydalidae), (e) Ithone fulva (Ithonidae), ( f ) Campion tenuistriga (Mantispidae), ( g) Psychopsis insolens (Psychopsidae), (h) Ceratoleon brevicornis (Myrmeleontidae), (i ) unidentified Peruvian Coniopterygidae, ( j) Porismus strigatus (Osmylidae), (k) Notobiella viridis (Hemerobiidae), (l ) Spermophorella sp. (Berothidae), (m) Stenobiella variola (Berothidae), (n) Dictyochrysa peterseni (Chrysopidae), (o) Glenochrysa opposita (Chrysopidae), and ( p) Norfolius howensis (Nymphidae). www.annualreviews.org • Phylogeny and Evolution of Neuropterida 533 EN63CH27_Engel ARI 20 November 2017 14:5 Cretaceous–Tertiary End PermianCarnian event Pluvial event Toarcian Extinction event Angiosperm radiation(K–T) boundary Eocene-Oligocene transition 350 300 250 200 150 100 50 0 Millions of years CarboniferousPermian Triassic Jurassic Cretaceous Paleogene Neogene PALEOZOICMESOZOIC CENOZOIC Coleopterida STREPSIPTERA COLEOPTERA Parasialidae Nanosialidae Priscaenigmatomorpha Chrysoraphidiidaeoraphidii Priscaenigmatidae Juroraphidiidae Raphidiomorpha BaBaissopteridae RAPHIDIOPTERA Metaraphidiidae Neuropterida Mesoraphidiidae Inocellidae Neoraphidioptera Raphidiidae Permithonidae Permoberothidae Sialidae MEGALOPTERA Corydalidae Coniopterygidae Conioptergyoidea Eidoneuroptera Sisyridae Nevrorthidae Osmyloidea Osmylidae Dilaridae Dilaroidea Euneuroptera Mesoberothidaeberothida Berothidae Mantispoidea Rhachiberothidae Mantispidae Ascalochrysidaeochrysida Solenoptilidae Osmylitidae Hemerobioidea Hemerobiidae NEUROPTERA Chrysopidae Neoneuroptera Ithonidae
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