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Home , Ascalaphidae, Campion (lacewing), Grammolingiidae, Mantispidae, Myrmeleontiformia, Myrmeleontoidea

EN63CH27_Engel ARI 20 November 2017 14:5

Annual Review of Phylogeny and Evolution of : 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 , California Department of Food and , 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, , 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. —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 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.

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INTRODUCTION Holometabolous are the paragons of biodiversity, with their numbers of and indi- Gula: a sclerite viduals dominating terrestrial ecosystems (34). The bulk of this species richness belongs to located ventrally on within the four megadiverse groups—Coleoptera, , , 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 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, , 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 ; 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 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 (70, 110) and supported it as sister to Coleoptera or Coleoptera + (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 but not primitive. In fact, most lineages of Holometabola diverged early in the or latest (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 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 and most extant families not known until the (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.

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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 ) and Megaloptera (shades of blue): (a) Eremoides bicristatus (), (b) Chasmoptera hutti (), (c) sp. (), (d ) Archichauliodes sp. (Corydalidae), (e) Ithone fulva (), ( f ) tenuistriga (), ( g) insolens (), (h) Ceratoleon brevicornis (Myrmeleontidae), (i ) unidentified Peruvian , ( j) Porismus strigatus (), (k) Notobiella viridis (), (l ) Spermophorella sp. (), (m) Stenobiella variola (Berothidae), (n) Dictyochrysa peterseni (), (o) Glenochrysa opposita (Chrysopidae), and ( p) Norfolius howensis ().

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Cretaceous–Tertiary End PermianCarnian event Pluvial event event Angiosperm radiation(K–T) boundary - transition 350 300 250 200 150 100 50 0 Millions of years CarboniferousPermian 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 Osmyloidea Osmylidae Dilaroidea Euneuroptera Mesoberothidaeberothida Berothidae Mantispoidea Mantispidae Ascalochrysidaeochrysida Solenoptilidae Osmylitidae Hemerobioidea Hemerobiidae NEUROPTERA Chrysopidae Neoneuroptera Ithonidae Ithonoidea Rafaelianidaeianidae

Annu. Rev. Entomol. 2018.63:531-551. Downloaded from www.annualreviews.org Nymphidae Geoneuroptera Nemopteridae Ascalaphidae Access provided by Texas A&M University - College Station on 01/28/18. For personal use only. BabBabinskaiidaei Myrmeleontidae Panfiloviidae Prohemerobiidae KKalligrammatidaeall Psychopsoidea Aetheogrammatidaetheogram Psychopsidae Osmylopsychopidaemylopsyc

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RAPHIDIOPTERA Snakeflies have the distinction of being the least diverse order among extant Holometabola, com- prising 248 modern species. They occupy a largely relict, circumboreal distribution, with their Exarate pupae: pupae greatest surviving diversity across the central Asiatic mountains (6, 7). Species occupy cooler habi- whose appendages are tats, either across the temperate zone or, for those extending southward into more tropical regions, not attached to the body and that are at higher elevations and are generally arboreal in all life stages, although some raphidiid larvae therefore fully mobile live in detritus, soil, or rock crevices. Pupae require an extended episode of cold to complete their development and are surprisingly mobile, active predators (exarate pupae), like the larvae and adults. Monophyly of Raphidioptera is supported by molecular studies and by various morpho- logical traits such as an elongate prothorax, giving them their snake-like appearance; a stout and elongate ovipositor; presence of a distinct pterostigma in the forewing; and a brief, subproximal fusion of the median vein (M) and anterior branch of the cubital vein (CuA) in the wings (34, 111, 120). Plesiomorphically, Raphidioptera retain a termination of the subcostal vein (Sc) into the costal wing margin, proximal to the pterostigma, and differ in this respect from most other Neuropterida. Most extant snakeflies belong to the Raphidiidae, a group consisting of 206 species in 26 genera and found in western North America, across Eurasia, and into the northern reaches of Southeast Asia. By contrast, comprise merely 42 species arranged in seven genera. The family is distinguished from Raphidiidae by the absence of both a pterostigmal crossvein and ocelli (7). Both families are represented by numerous Cenozoic (24), but neither is known prior to the Cretaceous–Tertiary (K–T) boundary, and together, they form a clade known as Neoraphidioptera (88). The real diversity for Raphidioptera resides within the Meso- zoic (24, 87, 118). Phylogenetic work on Raphidioptera remains in its infancy (36), but some rudimentary cladistic efforts have explored relationships among these Mesozoic groups (16, 53, 118). The earliest definitive snakeflies are species of the extinct suborder Priscaenigmatomor- pha from the to the mid-Cretaceous (24, 53), sister to all other Raphidioptera, or the Raphidiomorpha. The Mesozoic lineages of Raphidiomorpha constitute a grade relative to the Neoraphidioptera (Raphidiidae + Inocelliidae) (16, 53, 118). Importantly, these fossils not only represent a progressive series of stem groups to modern Raphidioptera but also demon- strate a once global distribution, as they are found in deposits throughout the Americas and Eurasia. No fossil snakeflies have been recovered from Mesozoic deposits in Africa or Australia, although they would be expected there. The uniquely Northern Hemisphere distribution and predilection for colder environments in extant Neoraphidioptera suggest them to be post-Eocene relicts. Widely overlooked are the clear raphidiopteran traits present in the Permian families Parasial- Annu. Rev. Entomol. 2018.63:531-551. Downloaded from www.annualreviews.org idae and Nanosialidae, traditionally considered as stem-Megaloptera. Of particular significance are the presence of distinct pterostigmata and a shared, subproximal fusion of M and CuA, features Access provided by Texas A&M University - College Station on 01/28/18. For personal use only. only present in Raphidioptera among Neuropterida and that implicate these Pararaphidioptera with the stem leading to Mesozoic Raphidioptera rather than Megaloptera.

←−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−

Figure 2 Phylogeny of Neuropterida mapped across a geological time scale, summarized from various recent sources (e.g., 15, 53, 111, 120) and showing best approximations of relationships among living and fossil families. Gray lines indicate observed ranges of extinct lineages or stem groups to surviving families, with thicker black lines documenting observed fossil records of putative crown-group clades. Major biotic turnovers are indicated, and pink highlights the period of angiosperm diversification.

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MEGALOPTERA There are presently 373 extant species of Megaloptera, including some of the largest Neuropterida, Decticous pupae: such as the 200-mm wingspan of Acanthocorydalis. Of the three orders of Neuropterida, only pupae whose Megaloptera have had their monophyly challenged (1, 3). Despite their individual peculiarities, mandibles are fully Megaloptera are, in many respects, rife with generalized traits, particularly their wings. Potential functional morphological synapomorphies for the order exhibit numerous reversals among various genera, and others represent loss of features. Nonetheless, nearly all modern analyses recover both Mega- loptera and its included families as monophyletic, and the presence of lateral abdominal gills in the is considered a synapomorphy for the order (14, 55, 112, 128). The aquatic specializations of larval Megaloptera are unique, and their invasion into freshwater habitats has been indepen- dent of those in Neuroptera. It is tenuous to homologize mere occurrence within freshwater as a historically heritable trait in the face of so many independent invasions across . Modern Megaloptera consists of two families, Sialidae and Corydalidae. Sialidae (alderflies) comprise 78 extant species in eight genera and are the smallest megalopterans, with wingspans of less than 30 mm. Sialids are generally distinguished from Corydalidae by the absence of ocelli and a dilated fourth tarsomere among adults, whereas as larvae, alderflies possess a distinctive caudal filament on the tenth abdominal segment and lack a pair of lateral gills otherwise present on the eighth segment (34, 54). Additionally, a partially desclerotized media posterior (MP) proximally located in the forewing is unique to Sialidae (5, 54). Fossil sialids are few but nonetheless include several Cenozoic records (54), with crown-group species as old as from the mid-Cretaceous (41). The earliest sialids are from the Jurassic, including wings from the Early Jurassic and larvae from the (5, 54). The family Corydalidae includes two reciprocally monophyletic clades and collectively encom- passes 295 extant species in 27 genera. Aside from lacking sialid traits, various synapomorphies in the genitalia support the family’s monophyly (55). Typically large and robust, corydalids also retain three ocelli, have the fourth tarsomere cylindrical, and, in the larva, have eight lateral gill pairs with prolegs on the distal segment and lack the caudal filament (34). Dobsonflies (Corydalinae), with their often spectacularly enlarged and ferocious-looking male mandibles, comprise 160 species compared to the 135 species of the somewhat smaller and less-daunting fishflies (Chauliodinae). Corydalinae have a high degree of sexual dimorphism, whereby males are larger than females and display greatly enlarged mandibles, whereas Chauliodinae do not exhibit such sexual dimorphism. Like snakeflies, the pupae are exarate and decticous (34). Fossil corydalids, mostly Corydalinae, are known from the Paleogene, with putative stem-group dobsonflies in the , whereas chauliodines are known from the (56, 108). 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. NEUROPTERA Neuroptera dominate the superorder in species richness, morphological diversity, and intensity of study (see the sidebar, Neuropterida in the Digital Age). Neuropteran monophyly has remained unchallenged, supported principally by larval morphology and anatomy (34, 46, 47). The larval mandibles and maxillae are interlocked to form jaws, which are used to suck fluids from prey or other food sources. Other unique features of the larva include a discontinuous gut, with the mid- and hindguts connected by a narrow tether and modification of the Malphigian tubules for production (120). Although the wings of most Neuroptera are immediately recognizable, there are no clear ordinal synapomorphies evident. For the last 40 years, the arrangement of families in Neuroptera has pivoted about a dichotomy into hemerobiiform and myrmeleontiform families (39, 40, 59). Monophyly of Myrmeleontiformia

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NEUROPTERIDA IN THE DIGITAL AGE

The study of Neuropterida is blessed by a portal through which all neuropterological information may be accessed. The Lacewing Digital Library, developed by John D. Oswald at Texas A&M University (83), is an online repository and database for the world’s literature, for the current classification to the level of species, and for evolving keys to families and genera, and a directory of past and present researchers. The value of this tool cannot be overestimated, and it should be the starting point for any neuropterological inquiry. Current extant species numbers for the families of Neuropterida quoted herein were all extracted from this singularly useful resource.

has rarely been questioned, but that of has been tenuous at best. This system was augmented on the basis of arguments placing the family Nevrorthidae as sister to - tiformia (8) and later to all other Neuroptera, resulting in a third suborder, Nevrorthiformia (9, 10, 14). Although initial studies using molecular data were unsatisfactory, lacking resolution and significant statistical support, they consistently recovered a paraphyletic Hemerobiiformia relative to Myrmeleontiformia and threw suspicion on a divergence for Nevrorthidae (35, 119). More expansive analyses of morphological and molecular data, including mitochondrial genomes, have demonstrated the of Hemerobiiformia and monophyly of Myrmeleon- tiformia and, importantly, placed Nevrorthidae back into an intuitive position among Osmyloidea (111, 120). In light of contemporary phylogenetic results, the long-standing subordinal system of Neu- roptera is ill equipped to reflect relationships and should be replaced with a series of more restricted groupings, especially subdividing Hemerobiiformia. Nevrorthiformia is particularly meaningless, as nevrorthids are sister neither to the remaining Neuroptera nor to Hemerobiiformia.

Basal-Diverging Neuroptera Coniopterygidae (dustywings) are the most atypical of Neuroptera, lacking the dense venation from which the order gets its name. All recent studies have recovered coniopterygids as sister to the remaining extant Neuroptera (or Euneuroptera) (111, 120), a placement consistent with the conclusions of Withycombe (123). Aside from molecular studies, the presence of plesiomorphic characters in female genitalic morphology and the number of Malpighian tubules place them outside of Euneuroptera (103, 104). Dustywing spermatozoa and ovariole ultrastructure are also divergent from other Neuroptera (48, 130, 131), but the significance of these, other than indicating

Annu. Rev. Entomol. 2018.63:531-551. Downloaded from www.annualreviews.org the family to be autapomorphic, remains to be fully explored. Coniopterygidae, encompassing 571 extant species in 23 genera, are minute, frequently under 7 mm in wingspan. Three subfamilies are

Access provided by Texas A&M University - College Station on 01/28/18. For personal use only. recognized—, Coniopteryginae, and the enigmatic Brucheiserinae from South America (67, 131). The integument of Coniopterygidae is covered with a waxy or mealy secretion, hence their common name, and their reduced wing venation is likely the result of miniaturization that took place sometime prior to the Late Jurassic, as definitive coniopterygids can be traced at least to the latter part of that period (68). The available Cenozoic fossils are easily assigned to extant tribes and even genera, whereas Mesozoic fossils only loosely fit within the current higher classification (26). Comparatively few phylogenetic studies have been undertaken on dustywings, with most morphological treatments produced in connection with the last monograph of the world’s fauna (67), although some recent accounts treated select character transformations of possible importance to coniopterygid evolution (92, 129). The single molecular analysis reflects relationships similar to those based on morphology (109).

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A Derived Dive: To Aquatic Larvae and Back Again Nevrorthidae and Sisyridae are united with Osmylidae as the superfamily Osmyloidea (or Hy- droneuroptera) and sister to all extant Neuroptera, excluding Coniopterygidae (111, 120). Sisyri- dae and Nevrorthidae have strictly aquatic larvae, whereas Osmylidae have larvae living in moist riparian habitats (except for one derived lineage of terrestrial larvae). Sisyridae have slightly more than 70 extant species in four genera worldwide and are known as spongillaflies, as the larvae feed on freshwater (Spongillidae) and bryozoans. The larvae are distinctive for their elongate, needle-like jaws and abdominal gills, both of which are unique among lacewings. Larvae subsequently emerge to build distinctive, open-mesh cocoons above the water line. Nevrorthidae (dragon lacewings) are found in areas of the Mediterranean, eastern Australia, and Asia, with 19 extant species in four genera (51). Originally proposed as a subfamily of Sisyridae, the discovery of their peculiar larvae led to their separation as a distinct family (132). Larvae are generalist predators found in clean, montane rhithral rivers and streams and, unique among Neuroptera, pupate in the water, constructing a distinctive cocoon that captures air within specialized pouches (63); the cocoon’s pocketed form resembles that of the open meshwork of Sisyridae. The larval head is supported ventrally by an elongate gula, superficially resembling that of Megaloptera and Raphidioptera (8, 17, 132). A gula, albeit utterly different, is also present in Ithonoidea + Myrmeleontiformia (59) and, along with eversible gland tubules on abdominal segments 6–8, was once believed to unite nevrorthids with the myrmeleontiforms. It is now clear that these evolved independently (111, 120). Adult nevrorthids and sisyrids are quite similar, with generalized patterns of wing venation that are sometimes difficult to distinguish, because of the retention of many plesiomorphies. Although the phylogeny of Sisyridae has yet to be explored, preliminary attempts have been made for Nevrorthidae (116). Osmylidae (lance lacewings) encompass 225 extant species in 30 genera; many are moderate to large lacewings typically with camouflaging patterns in the wings. The long, slender larvae with their elongate, lance-like jaws are generalist predators and live in riparian or drier subcortical habitats. The extant diversity is divided into two clades (122): Spilosmylomorpha (comprising the subfamilies Protosmylinae, Gumillinae, and Spilosmylinae) and Osmylomorpha (consisting of Os- mylinae, Kempyninae, Eidoporisminae, Porisminae, and a possibly paraphyletic Stenosmylinae). Those groups with larvae living near water are basal, and those with larvae from drier habitats are derived among the osmylomorphs (122). Nevrorthidae and Sisyridae have fossils dated to the mid-Cretaceous (61, 115), although nevrorthid-like larvae are found in the Middle Jurassic. Molecular age estimates give a range for the origin of stem groups to these lineages during the latest Permian to Triassic (120). Un- like sisyrids or nevrorthids, there is a comparatively rich fossil record for Osmylidae (122). The Annu. Rev. Entomol. 2018.63:531-551. Downloaded from www.annualreviews.org crown-group subfamilies are rather ancient, as representatives of definitive osmylomorphs and spilosmylomorphs are known from the Middle Jurassic (113, 114), and a putatively basal, extinct, Access provided by Texas A&M University - College Station on 01/28/18. For personal use only. and likely paraphyletic subfamily is known from the Late Triassic to mid-Cretaceous (43, 44). More peculiar are the Archeosmylinae and Saucrosmylinae, sometimes considered as separate families, the former ranging from the latest Permian to mid-Triassic and the latter from only the Middle Jurassic (29, 50, 97). These are perhaps stem-Osmylidae or even stem-Osmyloidea. The recently established Cratosmylinae (72) are likely nymphids (122).

Rearranging the Genome The small family Dilaridae, commonly referred to as pleasing lacewings, includes 80 extant species in five genera that are distributed widely in most biogeographical regions but are surprisingly ab- sent from Australasia (81). Most species are distinctive for the presence of sexually dimorphic

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antennae—females with long, filiform antennae, and males with pectinate antennae—and, in fe- males, for the presence of an elongate, somewhat arched ovipositor (76, 81), although both charac- teristics are reversed within the clade (52). Where known, larvae are predators of small arthropods and live subcortically or within soil, and like all Neuroptera discussed up to this point, with the exception of the specialized Nevrorthidae, have straight jaws that project forward and thus limit their grasping ability (75, 76, 120). The family has few fossil occurrences (23, 52), but, where known, these extinct species are all crown-group taxa and document the presence of the clade as far back as the mid-Cretaceous (52). Once considered the to the Mantispoidea in a combined unit referred to as the dilarid clade, the pleasing lacewings are basal to a large clade of all Neuroptera, excluding Co- niopterygidae and Osmyloidea (111, 120). This Cysneuroptera clade is noteworthy for a unique translocation in the mitochondrial genome whereby tRNACys is moved to an upstream position, an apparently unreversed change (111, 120, 127). Meanwhile, the dilarids are excluded from the remaining Cysneuroptera owing to the plesiomorphic retention of paired spermathecae and a complex of the bursa copulatrix and ductus seminalis, although this latter trait appears secondarily again in Psychopsidae and is lost in Coniopteryginae (103).

Mantispoidea and Raptorial Rapture The superfamily Mantispoidea encompasses three families—Berothidae, Rhachiberothidae, and Mantispidae, the latter two as reciprocally monophyletic sister groups (as the Raptoneuroptera) (117, 120). In the raptorial families, the profemora and protibiae are elongate and variously beset with spines used in prey capture (75, 117). Larval is also characteristic of this triumvirate. The Berothidae, widely known as beaded lacewings, comprise 113 species in 25 genera and are the most generalized among extant Mantispoidea. Berothids are found throughout the world, with their greatest diversity in Africa and Australia. Berothid biology is largely unexplored, but for those few where larvae are known (e.g., Isoscelipteron, ), they are predators of termites (Isoptera), feeding solely during the voracious first and third (45, 105). Phylogenetic relationships have been explored for the family on the basis of morphological data (13), and although fossil berothids are diverse and abundant, particularly in the Cretaceous (28), none have been included in such analyses. Paleogene berothids can be attributed to extant subfamilies, whereas the Mesozoic fossils do not correspond so clearly (28). Some compression fossils have been described in the extinct families Mesoberothidae and Mesithonidae (the latter a of the former) and together apparently form a stem group to either Berothidae or possibly even all other Mantispoidea.

Annu. Rev. Entomol. 2018.63:531-551. Downloaded from www.annualreviews.org Thorny lacewings, family Rhachiberothidae, are plesiomorphically similar to Berothidae and were first described as a peculiar, raptorial subfamily of the latter. The family has 13 extant species

Access provided by Texas A&M University - College Station on 01/28/18. For personal use only. in three genera, and although these are relict in sub-Saharan Africa (12), fossil rhachiberothines known from deposits are more diverse (25, 27, 66). Thorny lacewings are sister to Man- tispidae (117, 120), and this relationship supports a single origin of raptorial forelegs within the order. Phylogenetic relationships among the extant Rhachiberothidae have been studied (12), but expansion of such analyses to include the numerous fossil forms remains to be explored. The mantispid lacewings, or Mantispidae, are the most diverse and specialized of the raptorial lacewings, with 395 extant species in 44 genera. Aside from the grasping forelegs, their resemblance to is furthered by the presence of an elongate prothorax (76). Species are also noteworthy for their frequent evolution of mimetic forms and color patterns, typically resembling brightly colored vespid (e.g., Euclimaciella) or cantharid (Calomantispa) (76). Relationships among the four extant subfamilies have been explored using morphological and limited molecular

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data, all of which indicate a derived placement of relative to other lineages (49, 57). Indeed, whereas Mantispidae extend back to the Jurassic, mantispines may scarcely predate the K–T boundary (57). Crown-group Mantispidae are known throughout the Cenozoic (27). Jurassic and Cretaceous mantispids, sometimes misidentified as primitive chrysopids, likely represent stem groups to the modern subfamilies, or perhaps even all Raptoneuroptera. Once considered as a distinct family, Dipteromantispinae were exclusively Cretaceous mantispids with hind wings reduced to haltere-like structures (62). No attempt has been made to integrate the available fossils into existing cladistic analyses for the family. Regardless, the close relationship of Mantispidae and Rhachiberothidae combined with their respective fossils demonstrate the great antiquity of raptorial prey capture among Neuroptera.

From Straight to Curved Jaws: The Better with Which to Eat A relationship between Hemerobioidea, Ithonoidea, and Myrmeleontiformia has been long sur- mised, evidenced by the shared presence of arched larval jaws widely separated at their bases, coupled with modifications of the head capsule used to reinforce it during powerful movements in either grasping/seizing prey or digging through tough plant tissues (120, 123). All clades discussed up to this point have straight, forward-directed jaws whose articulations are closely approximated on the front of the head (Figure 3); Nevrorthidae are unique in that they have straight jaws that are curved at the tip only (17, 76, 132). Hemerobiidae and Chrysopidae form a putatively monophyletic group as superfamily Hemer- obioidea (11, 35, 111, 120), but in some analyses, this association falls apart (10, 14). Both have similar, rather generalized campodeiform larval forms, with subtriangular heads supported by postoccipital apodemes that converge posteriorly to form a prominence and have trumpet-shaped pretarsal empodia in at least the first (59, 123). Other clear synapomorphies have been elu- sive, and adults show little similarity between the two families. Hemerobiidae (brown lacewings) comprise 591 species in 28 genera found throughout the world. Like larvae of chrysopids, brown lacewings are generalist arboreal predators (75). Adults are small with variable wings, including the repeated evolution of brachypterous and flightless forms (32, 77, 79, 80). When wings are present, they assume a variety of shapes but are most well characterized by the peculiar possession of multiple oblique radial sector (Rs) branches arising directly from the first radial branch (R1) (79). The earliest hemerobiids are those from the Late Jurassic (79), an age that corresponds well with known chrysopid fossils (2), with other fossils known from the Early Cretaceous through the (27, 60, 79, 82). The closely related green lacewings, family Chrysopidae, are one of the largest radiations among

Annu. Rev. Entomol. 2018.63:531-551. Downloaded from www.annualreviews.org Neuroptera, with 1,415 extant species arranged in 81 genera. The larval body differs from those of Hemerobiidae in the presence of elongate, trumpet-shaped pretarsal empodia in all instars,

Access provided by Texas A&M University - College Station on 01/28/18. For personal use only. and the presence of various protrusions and anchoring setae (76), which, in some species, are used to hold a packet of exogenous materials (106). The packet serves as camouflage and physical defense against predators, parasites, and conspecific cannibalism (106). Larval camouflaging has apparently evolved once within the family, with several subsequent losses, and its origin extends into stem-group subfamilies (85, 86, 106, 107). Adults are similarly distinctive, and although there is a generally uniform chrysopid habitus, there is considerable variation within the family (19). In particular, chrysopid wing venation is one of the more characteristic among Neuroptera and includes some complex patterns of fusion among the longitudinal sectors to form composite veins (19). Whereas extinct families like Solenoptilidae, Ascalochrysidae, and Osmylitidae, and stem- group subfamilies such as Mesochrysopinae, display characteristics of modern chrysopids, they

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a b

c d e

f g 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.

Stipes Cardo Postmentum Prementum Gula

Figure 3 Larval heads in ventral aspect with the arrangement of sclerites colored. (a) Polystoechotus punctatus (Ithonidae), (b) Corydalus cornutus (Corydalidae), (c) Austronevrorthus sp. (note that the postmentum is divided into mentum and submentum) (Nevrorthidae), (d ) americanus (Coniopterygidae), (e) Nodita pavida (Chrysopidae), ( f ) quadrimaculata (Ascalaphidae), and ( g) viridis (Mantispidae). Redrawn from Reference 59 except for panel c, which was redrawn from Reference 17.

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still retain primitive wing features of related families in Neoneuroptera (e.g., 96), representing a grade of intermediate groups linking the Neoneuroptera with the specialized modern subfamilies of Nothochrysinae, Apochrysinae, and the highly diverse and species-rich . Fossils attributable to Apochrysinae are lacking, but chrysopines and nothochrysines are known from throughout the Cenozoic (2, 19), although none of the extant subfamilies extend beyond the K–T boundary. The extinct chrysopid subfamilies Mesochrysopinae and Corydasialinae are sometimes considered as separate families (e.g., 58), but such an arrangement seems to be an artificial in- flation of higher groups, obscuring their relationship to crown-group Chrysopidae. On the basis of their relative abundance as fossils, and presumed plesiomorphic characteristics, the subfamily Nothochrysinae has been considered the most basal among crown-group green lacewings, with Apochrysinae and Chrysopinae presumably more derived sister groups (19). Recent phylogenetic evidence based on morphology and molecular data is equivocal, recovering all possible relation- ships among the three subfamilies (21, 22, 37).

Going to Ground: Geoneuroptera The hypothesis of Ithonoidea and Myrmeleontiformia as extant sister groups (herein Geoneu- roptera) was advocated by MacLeod (59) based on larval data and has been supported by recent combined morphological and molecular analyses (120). Geoneuroptera is supported by, among other traits, an unpaired arcessus and, more notably, the presence of a gula in the larval head cap- sule (59, 120). In both groups, the gula appears as a small structure between the occipital foramen and the base of the postmentum (59). In derived Ithonidae, such as Ithone, the gula is reduced to a series of small gular sclerites, and in Myrmeleontiformia, the gula is of triangular shape (59). As mentioned previously, this form of gula differs quite dramatically from the elongate gula of Nevrorthidae, which separates the opposing postgenae (Figure 2). The larvae of this clade are found in the soil or detritus, although notable exceptions of arboreal larvae do occur in unrelated genera of Psychopsidae, Nymphidae, Myrmeleontidae, and Ascalaphi- dae. The widespread taxonomic occurrence of surface-dwelling larvae across the Ithonoidea + Myrmeleontiformia tends to imply that this is ancestral to the clade and a defining feature of the group, with those arboreal taxa putatively representing secondary specializations. The deep subterranean habit of Ithonidae represents a specialization of that family alone.

A Phytophagous Congregation Unique among the otherwise predatory Neuroptera, Ithonidae (Phytoneuroptera) are a group of

Annu. Rev. Entomol. 2018.63:531-551. Downloaded from www.annualreviews.org specialized phytophagous or saprophagous lacewings (30, 31), with 39 extant species in 10 genera. Observations on the Australian Ithone provide compelling evidence that the larvae are phy-

Access provided by Texas A&M University - College Station on 01/28/18. For personal use only. tophagous root feeders (31). The scarabaeiform, fossorial larvae and generalized adult form led many to consider ithonids as sister to all other Neuroptera (123), or at least basal among Hemer- obiiformia (14, 33). The larval jaws are short, arched, and comparatively broad (33, 59). Adults are distinctive for their generally robust form, medium to large size, and occasionally multiple Rs origins. Traditionally, Ithonidae were restricted to a set of robust, hairy genera, frequently dubbed as moth lacewings, found in Australia, montane Central America, and the southwestern United States. A combined analysis of molecular and morphological data for living and selected fossil gen- era demonstrated ithonid paraphyly relative to the New World Polystoechotidae and montane Southest Asian Rapismatidae, and they are now all united as one (121). Fossil ithonids span the Late Jurassic to Early Eocene (121), whereas Middle Jurassic species described as polystoechotids (95) are likely stem-Ithonidae, or perhaps even stem-Geoneuroptera.

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The Psychopsoid and Myrmeleontoid Families The five extant families of Myrmeleontiformia constitute one of the least controversial nodes in neuropteran phylogeny, and our understanding of their relationships has changed little since Dolichasters: Withycombe’s (123) pivotal monograph (15, 39, 64). Myrmeleontiform monophyly is largely sup- modified, elongate ported by unique larval specializations, most notably the presence of dolichasters, a hypostomal setae with crown- or star-like apexes bridge [the gular line of MacLeod (59)], and distinctly separated premental elements (15, 59). Withycombe’s (123) stepwise set of relationships—with Psychopsidae, Nemopteridae, Nymphi- Vena triplica: a characteristic close dae, Ascalaphidae, and Myrmeleontidae forming a pectinate series—has been augmented recently, + approximation of the with Nemopteridae as either sister to Ascalaphidae Myrmeleontidae (111, 120) or, less con- subcostal vein (Sc), R1 vincingly, Psychopsidae (11, 14). The extant Myrmeleontiformia give a misleading approximation branch, and radial of their real historical diversity, with numerous extinct families from the Mesozoic (Figure 2), sector (Rs) along their including some of the most impressive lacewings ever to have lived. length and usually closed apically by Psychopsidae (silky lacewings) are plesiomorphic relative to other myrmeleontiforms, no- crossveins or fusion at tably so in the larvae, with long antennae and five stemmata in the eye and lacking mandibu- the same position lar teeth (15). Adults are distinctive for their broad, densely setose and patterned wings, with a wide costal field and characteristic vena triplica (78). Larvae are rarely encountered, although those of Psychopsis are known to live as generalist predators under bark (75). The family is sis- ter to all other Myrmeleontiformia and forms the superfamily Psychopsoidea along with a series of extinct families extending from the Triassic to the Cretaceous (Figure 2). The putatively most basal are the Panfiloviidae (including as a subfamily), lacking the vena triplica of the remaining psychopsoids but sharing the broadly constructed costal field. Pro- hemerobiidae (including Parakseneuridae as a subfamily) are more generalized Jurassic forms with similarities to Ithonidae (124) and might represent stem-Myrmeleontiformia rather than Psychopsoidea. Aetheogrammatidae and were two of the more impressive families, with large, patterned wings and elongate mouthparts (94, 125). Osmylopsychopidae (including Brongniartiellidae) are the most clearly psychopsid-like of these families (84) and may represent a grade to modern psychopsids. The earliest psychopsid is apparently Trias- sopsychops superbus from the Late Triassic of Australia, although the genus and other Meso- zoic Psychopsidae are stem taxa, with crown-group Psychopsidae appearing in the Cenozoic (4, 78). All other families are united into the Myrmeleontoidea, supported by the possession of an enlarged and ventrally flattened premental element in larvae (15). Basal within this group are the split-footed lacewings—family Nymphidae—which cover 35 species in eight genera of relict, Aus- tralasian distribution. Nymphids are distinctive for a characteristically split arolium and thyridiate subcostal crossveins in the forewings (99). The predatory larvae have broadly separated jaws and Annu. Rev. Entomol. 2018.63:531-551. Downloaded from www.annualreviews.org are either cylindrical with short, lateral scoli on the thorax and abdomen (Nymphinae) or are broadly flattened, with elongate scoli (Myiodactylinae). Where known, nymphine larvae con- Access provided by Texas A&M University - College Station on 01/28/18. For personal use only. struct a packet of exogenous materials to cover the body and live in detritus or soil, whereas myiodactylines do not and are arboreal. Nymphid phylogeny has been estimated using molec- ular and morphological data, including available fossils, and supports reciprocally monophyletic subfamilies, whereas the extinct family Nymphitidae nests within a grade of fossil nymphines (99). Nemopteridae are highly distinctive lacewings, with characteristically narrowed and elon- gate hind wings. Two subfamilies are recognized: Crocinae (thread lacewings, 48 species) and Nemopterinae (ribbon- or spoon-winged lacewings, 98 species). Crocinae are generally smaller with narrow, threadlike hind wings. They are largely nocturnal or crepuscular and live in arid zones where their peculiar long-necked larvae typically live in caves, under stones, or in crevices

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(71). The larger, diurnal Nemopterinae have their hind wings apically dilated, and those of males often bear a bulla (76). Nemopterine larvae lack the elongated neck found in crocines and burrow headfirst into sand or soil where they consume their prey underground. Only a single study has Bulla: a patch of setae set into a depression recently explored relationships among the diverse nemopterine fauna of South Africa (100), and on a thickened vein, the family is widely recognized as monophyletic (15, 64); although this was not found in two putatively serving as a analyses (17, 91). The earliest nemopterids are from the Early Cretaceous of Brazil and have hind sex organ wings similar to those of Crocinae (65). Nemopteridae have been supported as sister to Ascalaphi- dae + Myrmeleontidae in combined phylogenetic analyses (120), and the complete fusion of the posterior portion of MP and the anterior branch of CuA appears to be a good synapomorphy uniting these three families (69, 98), although reversed in some taxa (42). Antlions (Myrmeleontidae) are the most species-rich family of Neuroptera, with nearly 1,660 extant species in 198 genera worldwide. larvae are typically found in friable soils, in leaf litter, and on rocks. Larvae of the tribe dig the characteristic conical pits in sandy soils where they wait at the bottom for unsuspecting prey to tumble therein (75). A close relationship between Myrmeleontidae and Ascalaphidae is widely accepted (15), although some recent molecular studies suggest paraphyly of Myrmeleontidae relative to Ascalaphidae (111, 120). Myrmeleontid fossils are available from the Early Cretaceous to the Miocene (27, 93). A series of Mesozoic genera that are seemingly stem-Myrmeleontidae at times have been considered distinct families (65, 69) but are better considered extinct subfamilies at the base of crown-group Myrmeleontidae. Owlflies (Ascalaphidae) are characterized by elongate antennae with a distinctive apical club, by usually more robust and setose bodies, and, in larvae, by prominent occipital lobes and jaws with three stout teeth (76). The family includes 431 extant species in 100 genera and three subfamilies— , Haplogleniinae, and the monospecific Albardiinae of South America (74, 76). Larvae may be either terrestrial or arboreal, feeding on other insects on the ground (Ascalaphinae and Albardiinae) or on vegetation (Haplogleniinae). Little phylogenetic inquiry has been attempted within Ascalaphidae, although the division of the compound eyes in Ascalaphinae perhaps con- firms this subfamily’s monophyly. Besides the distinction of subfamilies, relationships are largely unknown, and this family is a priority for more comprehensive studies at all levels. The fossil record of Ascalaphidae is poor in comparison to many other Myrmeleontoidea, with adults and larvae of modern genera known from sundry Cenozoic localities (27) and a single record from the Early Cretaceous. Divergence time estimates suggest that the common ancestor of Myrmeleontidae and As- calaphidae diverged from the ancestor of the nemopterid lineage during the mid–Late Jurassic and that modern antlions emerged during the Cretaceous (69, 111, 120). This is unique among

Annu. Rev. Entomol. 2018.63:531-551. Downloaded from www.annualreviews.org lacewings because all other families are of considerably greater antiquity. Access provided by Texas A&M University - College Station on 01/28/18. For personal use only. NO EPILOGUE, I PRAY YOU The systematization of any group is a seemingly endless task. The discoveries of new species, living or fossil, or hitherto unknown life stages or natural histories, provide a constant source of data from which to expand future analyses. These either corroborate or refute—we hope for the former—prior estimates of relationship and the classifications they underpin, and through this iterative process, the science progresses. In time, our own account may be found wanting in certain respects, although we take some assurance in the convergence of multiple sources on a common theme. Regardless, neuropterology is today a robust field, and we look forward to the discoveries awaiting the latest generation romanced by diaphanous wings of lace.

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FUTURE PROSPECTS 1. Expanded phylogenetic efforts are needed throughout the families of Neuropterida, par- ticularly Coniopterygidae, Sisyridae, Berothidae, and Ascalaphidae, as well as studies that move beyond the usual passe´ character systems. 2. Widely ignored characters need to be more richly explored, including ethological vari- ation and internal anatomy, such as the plethora of glandular systems and associated semiochemicals. 3. Using transcriptomes, the underlying genetic architecture for particular phenotypes needs to be identified, bolstering the genotype–phenotype link, clarifying putative ho- mologies, and building an evo-devo perspective toward lacewing evolution. 4. The rapidly growing body of fossil evidence needs to be more integrated into large-scale analysis not only within families, but at the higher level across and among the orders.

DISCLOSURE STATEMENT The authors are not aware of any affiliations, memberships, funding, or financial holdings that might be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS We are indebted to those pioneers who have done much to make our own neuropterology meaning- ful and whose labors set the foundation upon which we have erected our scaffolding. In particular, we owe much to two who only recently left us—Norman D. Penny (1946–2016) and Maurice J. Tauber (1931–2014). In addition, we are grateful to the Editorial Committee of the Annual Review of Entomology for the invitation to provide this overview, to S. Tanamachi for his expert assistance and patience, and to C. Barbera for her great assistance with the article. This review has been supported by US National Science Foundation (NSF) grants DEB-1144119 (to S.L.W.) and DEB-1144162 (to M.S.E.). Statements and viewpoints expressed herein do not necessarily reflect the opinion of NSF. This is a contribution of the Division of Entomology, University of Kansas Natural History Museum. Annu. Rev. Entomol. 2018.63:531-551. Downloaded from www.annualreviews.org LITERATURE CITED

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