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13

Diversity and Significance of : A Phylogenetic Perspective Paul Z. Goldstein

Systematic Entomology Laboratory, Science Institute, Agriculture Research Service, US Department of Agriculture, c/o Smithsonian Institution, Washington, DC, USA

The Lepidoptera – , , and skip- aggressive . Ecologically, butterflies and pers – represent one of the three most ‐ moths constitute a primary food source for diur- rich orders and the largest evolutionary nal and nocturnal vertebrate insectivores, serve radiation of herbivorous (Scoble 1992, as hosts for innumerable specialist insect parasi- Wahlberg et al. 2013). The origins of the toids, and have important roles as pests and pol- Lepidoptera make it the youngest of the five linators, acting as both agents and objects of mega‐diverse insect orders, the others being natural selection. Having coevolved with preda- Coleoptera, Diptera, Hymenoptera and tors and host , butterflies, moths, and their Hemiptera – all except the last united within the larvae represent a significant component of ter- Holometabola. Although most lepidopterans are restrial , and their herbivory has confined to vegetative substrates and display influenced the evolution of plant defensive perhaps the narrowest collective diet breadth of mechanisms. They are an important forum for these groups, most of the higher phylogenetic exploring ecological and evolutionary questions diversity arose in association with the diversifi- surrounding the mechanics of speciation, natu- cation of flowering plants during the ral selection, and mimicry, and the roles of (Powell et al. 1999, Grimaldi and Engel 2005), chemistry and climate shifts in the evolution of paralleled by the diversification and spread of life histories. mammalian predators and insect . From the societal standpoint, lepidopterans Their morphological, physiological, and behav- provide obvious resources, being perhaps ioral innovations for capitalizing on chemically the most obvious of these, but they also number defended food plants and for avoiding and deter- among the most destructive and economically ring predators have made Lepidoptera major important forest and agricultural pests. Many components of the evolutionary landscape, and species are candidates for combating invasive they represent an important nexus for studying plants and, along with beetles, moths represent the history of life. Lepidopteran larvae, whether one of the most commonly tapped orders for exposed feeders that graze externally or con- biocontrol agents (Weed and Casagrande 2011). cealed as miners, leaf rollers, and stem bor- Because they respond quickly to environmental ers, stand out among the holometabolous change, including climatic and atmospheric as conspicuous participants in the evolutionary shifts and landscape alteration, Lepidoptera dynamics of defensive behaviors, , and serve as a means of detecting systemic threats to

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd. 464 Insect Biodiversity: Science and Society

biological resources and as an early‐warning the chapter’s remaining core, I review current ­system for ecological degradation. They include understanding of how species diversity is distrib- some of the more well‐known threatened and uted across major lepidopteran groups and some endangered species. Butterflies and moths also of the more conspicuous biological innovations include some of the most conspicuous and beau- with which evolutionary bursts of diversification tiful insects, and represent a common gateway might have been associated – the various groups’ group through which children and young adults evolutionary highlights, so to speak, from within develop an understanding of natural history and the context of their phylogeny as we understand of entomology in particular. More broadly, but- it. Because lepidopteran classification remains in terflies and moths have figured prominently in flux, I also highlight the more significant recent religious and spiritual frameworks and as sym- changes in classification, reflecting advances in bols of beauty, frailty, and spirit in the works of the inference of lepidopteran phylogeny. Although artists and writers for millennia (Nazari 2014). the emphasis of this discussion is phylogenetic, I Yet there is a duality in how Lepidoptera are per- also stress the geographic distribution of lepidop- ceived. The charisma of butterflies is perhaps teran species richness, and the research direc- matched by a more mundane and darker mystique tions, challenges, and opportunities that a better surrounding their nocturnal relatives. Beyond understanding of that richness presents. their banal use in metaphor (“moths to a flame”) and their association with closet and wardrobe pests, moths are often used to represent agents of 13.1 Relevance of Lepidoptera: the macabre in popular culture, as in films such as Science Silence of the Lambs or The Mothman Prophecies. Lepidopterists have embraced this mythos, gener- Lepidoptera have provided signature examples ating common names and taxonomic appellations of numerous biological phenomena and, in many associated with darkness and death, as in “death’s‐ cases, the impetus for the development of head hawkmoth.” Reflecting the duality of popular inquiry, including the physiology of metamor- perception is an asymmetry in the popular under- phosis and diapause, the existence of mimicry standing of lepidopteran and diversity: and , chemical ecology and coevo- butterflies are rarely understood as simply a lution, mutualisms and tri‐trophic interactions, derived subset of moths, nested within more than the chemical mediation of diet breadth and die- 40 other superfamilies. The common question tary specialization, and the mechanics of specia- “What’s the difference between butterflies and tion and sexual selection. Early demonstrations moths?” brings shudders to zoologists in the same of natural selection were grounded in empirical way as asking the difference between rabbits and research of butterflies and moths, and in many mammals. But most importantly for present pur- of these arenas, Lepidoptera have enjoyed sus- poses, the relationships among many of these tained pre‐eminence. The discovery of lock and groups, including butterflies, remain poorly key mechanisms in genitalia (Eberhard understood and are often controversial. 1985, Shapiro and Porter 1989, Mikkola 2008, I first briefly outline the more conspicuous ways reviewed by Masly 2012) and of sphragides in which Lepidoptera intersect with human soci- (“chastity belts”), which are widely distributed ety via culture, agriculture, and natural resource in butterflies (Ehrlich and Ehrlich 1978), have conservation, and particularly the roles they play ­illuminated the mechanisms of sexual selection in the scientific study of evolutionary and ecologi- and sperm competition, respectively. The cal phenomena. Next, I review some of the cur- respective roles of chemistry, rent directions and challenges, ­epitomized in the ­phenology, and diurnality promise to be equally study of Lepidoptera, when it comes to docu- valuable in the study of disruptive selection and menting and understanding species diversity. In allochronic speciation. 13 Diversity and Significance of Lepidoptera 465

Lepidoptera have provided some of the most a unique role in the development of genomic col- high‐profile examples of both diffuse and strict lections and phylogenomic studies. In North coevolution. The more well‐studied examples America, DNA barcodes have been obtained for include the mimicry complex among Heliconius more than 95% of the macrolepidopteran fauna butterflies (; Gilbert 1984, Brower (Zahiri et al. 2014). To the extent that fresh speci- 1996), dioptine prominent moths (; mens can be determined reliably in the field, 1996, 2009), and other winged insects, genome‐grade tissues may be amassed more effi- many of which share passion ciently than for many invertebrate groups, and (Passifloraceae) as larval hosts. Yucca and yucca phylogenomic progress is likely to be rapid in moths () include some of the few Lepidoptera. demonstrable examples of strict coevolution, if Perhaps more than any insect group, Lepidoptera not cospeciation (reviewed by Pellmyr 2003). feature prominently among species under legal The study of Lepidoptera has illuminated the protection and in various conservation programs chemical mediation of diet breadth and dietary and habitat restoration projects. Although a great specialization over evolutionary time, and the deal of effort and research has focused on the con- role of chemistry in the origins of aposematism servation of particular species or assemblages of mimetic systems. Some of these studies have in butterflies and moths, Lepidoptera have an impor- turn led to advances in our understanding of tant role in highlighting systemic threats to natural insect vision and bioacoustics in larval and adult and aiding the assessment of conservation insects. Genes responsible for vision priorities. Growing recognition of the sheer mag- have been shown to be under positive selection nitude of biological diversity has necessitated a where wing patterns are involved in both more refined approach to conservation than Müllerian mimicry and kin recognition (Briscoe focusing exclusively on individual species, and et al. 2010, Bybee et al. 2012). So‐called “singing Lepidoptera present themselves as useful tools, ” (DeVries 1991) communicate with rather than simply targets, of conservation efforts. by means of acoustic signaling as a defense The utility of Lepidoptera in evaluating the stabil- against parasitoids, and acoustic aposematism ity of biological communities derives, in many seems to have evolved independently in multiple areas, from how well known the faunas are and lepidopteran groups (Brown et al. 2007). Adult from the availability of comparative to assess sphingid and saturniid moths have evolved rarity and uniqueness. But more generally, butter- means of foiling bat sonar to avoid bat and moths have long been recognized to (Barber and Kawahara 2013, Barber et al. 2015), respond rapidly to climate and landscape‐level and adults of the most diverse lepidopteran changes, anthropogenic and otherwise. In the past groups ( and ) are not only decade, observers have noted the northward equipped with sonar‐detection but also, in some spread of species, an increase in the number of cases, have themselves evolved acoustic apose- generations per year, and the contraction of spe- matism (Barber and Connor 2007, Conner and cies restricted to high‐altitude or montane habi- Corcoran 2012, Corcoran et al. 2009), warding tats, apparently in response to climatic temperature off their would‐be predators with sound instead shifts and prolongation of growing seasons of, or in addition to, bright colors. Because they (reviewed by Parmesan 2006). can be sampled readily, butterflies and moths are common foci of community ecology and faunis- tic studies. Likewise, as they have been well‐col- 13.2 Relevance of Lepidoptera: lected and documented in many regions Society (especially and Europe), Lepidoptera from these areas are among the Lepidoptera account for some of the most eco- most readily identified and vouchered, and have nomically and agriculturally significant examples 466 Insect Biodiversity: Science and Society

of forest, agricultural, and stored‐product pests, somewhat vague. As Wilson himself decried in a many of them outbreak and invasive species. The different context while championing the use of a accidental introduction of forest pests and our more rarely used word (consilience), loss of pre- responses to them have had repercussions for cision accompanies popularity of usage, and native faunas. The introductions of the gypsy words often see their intended meaning diluted moth dispar and the browntail moth through overuse. Biodiversity may have become chrysorrhoea (both ), and more such a word, in that its meaning – and rele- recently the winter moth Operophtera brumata vance – are at risk of being overshadowed by its (Geometridae), have incurred enormous costs to caché. Nevertheless, the quantification of bio- North American forests. The systemic non‐target logical diversity has been the subject of many impacts of pesticide deployment (e.g, of dichlo- empirical and theoretical works from faunistic, rodiphenyltrichloroethane (DDT) and carbaryl ecological, genetic, and phylogenetic perspec- (Sevin)) and of parasitoids introduced as biocon- tives. In view of its varied usage, I use the term trol agents, such as the biodiversity sparingly but embrace its vague- (; Boettner et al. 2000), have likewise ness to convey meaning that transcends raw been immeasurable. numbers of species and includes as wide a Caterpillars, especially those of , breadth as possible of behavioral, ecological, , and Pyraloidea, are some the most and genetic richness. frequently intercepted agricultural pests and elicit That said, and with full recognition that the quarantine actions on fresh produce and stored meaning of biodiversity defies simple quantifica- products entering the United States from abroad. tion, I stress that any interpretation of species rich- Specialist lepidopteran are frequently ness rests ultimately on some criterion for what screened in the development of biocontrol pro- constitutes a species in the first place and, as is the grams to target invasive plants, such as the case elsewhere in biology, such issues abound in Brazilian pepper tree Schinus terebinthifolius entomology generally and in Lepidoptera particu- (Manrique et al. 2012) and black swallow‐wort larly. The centuries‐old debate over the ontology Vincetoxicum spp. (Hazelhurst et al. 2012), the of species has been largely metaphysical and often latter of which has been implicated in declines of semantic, focused on how best to define entities monarch butterflies by acting as a potential ovi- assumed to have some essentialist nature beyond position sink (Casagrande and Dacey 2007). The or independent of our detection. And as with all unchecked, transcontinental spread of the pyralid metaphysical debates, this one has led nowhere moth Cactoblastis cactorum, originally employed except to demonstrate that scientists operating as a biocontrol agent for prickly pear Opuntia in under different premises inevitably reach different , now threatens numerous cactus species conclusions. Rather than perpetuate or recapitu- (Stiling 2002). late such discussions here, I will for the sake of clarity (and, from this point forward, brevity) pre- 13.3 Diversity and Diversification: sume a certain fundamental consensus on the that at least broadly consistent criteria for diag- A Clarification of Numbers nosing species enable our ability to explore them and Challenges scientifically and classify them efficiently. Whatever their essence, species occupy unique This chapter is devoted largely to documenting roles in the taxonomic hierarchy as benchmarks the state of our understanding of species diver- that differentiate the empirical, phylogenetic sity. “Biodiversity” is a term that gained popu- framework of classification from the study of larity after Wilson (1988) used it to refer to the microevolutionary change within populations. panoply of taxonomic, biological, and behavio- This distinction, while easily blurred by the ral richness, but its definition has since grown increasingly routine use of molecular genetic 13 Diversity and Significance of Lepidoptera 467 tools in taxonomic and phylogenetic studies, reflecting historical events. Comparative analy- bears directly on our appreciation of species sis of shared behavioral, anatomical, and physi- richness in Lepidoptera, nowhere more appar- ological features enables us to understand their ently than in the use of mitochondrial DNA bar- mechanics and to disentangle independent ori- codes to identify cryptic species. In perhaps no gins of superficially similar attributes from of insects has the use of DNA barcodes those attributable to singular ancestral events. been more extensively applied than in the The historical dimension of taxonomy and Lepidoptera (Hajibabaei et al. 2006, Rougerie classification underlies its power not only to et al. 2014). As has been the case in other insect arrange, but also to explain biological diversity, groups, such studies have uncovered species but there lingers a more one‐dimensional view diversity far exceeding that already described. of systematics as a technical discipline confined The focus below is confined to assessing how to the formulaic business of describing and nam- species diversity is distributed among recog- ing species. As growing threats to biological nized higher lepidopteran taxa, and how these diversity have been accompanied by dwindling components of lepidopteran biodiversity are resources available to document it, so too has associated with behavioral and morphological concern that the pace of taxonomic progress is innovations. inadequate to document biological diversity before most of it disappears. Often, such argu- ments involve the so‐called taxonomic impedi- 13.4 State of Lepidopteran ment as an obstruction to scientific progress. For Systematics and better or worse, Lepidoptera are among those taxa at the forefront of lively discussions and Biological species richness defies one‐dimen- debates over ways to overcome the taxonomic sional abstraction. Our tendency as biologists is impediment – commonly misinterpreted as a to equate evolutionary “success” with species shortcoming in the field of systematics, as richness, as if it reflects longevity or endur- opposed to an indication of the sheer magnitude ance – we often equate a net increase in specia- of biological diversity remaining to be described. tion with some notion of collective fitness, and The past decade has seen proposals to amend or not simply with a propensity for rapid repro- upend the Linnaean system of hierarchical clas- ductive isolation that generates many species, sification in favor of molecular taxonomy, to but short‐lived ones. Species‐rich groups are bypass nomenclatural codes in favor of democ- commonly attributed to one or more evolution- ratized registries, and to replace rigorous diag- ary novelties or key innovations, but these are noses with heuristic distance‐based measures rarely tested empirically. A complementary that impede comparative analysis. Some have view is that each extant species represents a his- even used the rate of species and torically unique entity, not only a unique collec- descriptions to argue that taxonomy is flourish- tion of behaviors and adaptations but a genome ing (Costello et al. 2013), again as if the endeavor that has evolved and survived the filter of of systematics is a one‐dimensional descriptive extinction events and bears clues for decipher- exercise devoid of empirical strength. ing biological and evolutionary history through As in other groups with conspicuously pat- its relationships with other organisms. This is terned organisms, butterflies and some of the the essence of comparative biology: that biolog- more showy moth groups have received a great ical classification represents not simply a collec- deal of taxonomic attention at the species level, tion of unique identifiers used for determining which perhaps has diverted attention from specimens, nor simply a mnemonic system of higher‐level phylogenetic research toward what is categorization and information storage, but a seen as the taxonomic impediment. Although set of testable hypotheses of relationships most practicing systematists have come to eschew 468 Insect Biodiversity: Science and Society

the description of subspecies, historical prolifera- evolutionary novelties in their ancestral food tion of subspecific and infrasubspecific epithets plants, but accelerated by changes in dominant in Lepidoptera has been conspicuous and these vegetation responding to climatic change efforts have been viewed by some as having (Goldstein and Fibiger 2005), such as the origin drained attention and potential expertise from of C4 grasses and the spread of grasslands dur- comparative higher‐level studies. Kristensen et al. ing the Miocene (Toussaint et al. 2012). (2007) suggested that the study of higher‐level It is interesting to observe parallel debates over lepidopteran relationships (among superfamilies, which side of the Cretaceous–Paleogene bound- for example) has been compromised by the ary major groups of Lepidoptera and other organ- group’s charisma. He articulated two mutually isms (bats, for example) evolved. But in some reinforcing tendencies in which (i) lepidopteran cases the question is currently untestable, either wing scales – the feature responsible for the beau- because lepidopteran are rare (Sohn et al. tiful but distracting color patterns – obscure 2015) or because we cannot differentiate whether important structures relevant to deciphering phy- mass extinctions, the causes of mass extinctions, logenetic relationships except at the species level, or the biological vacuum resulting from mass and (ii) the more promising entomologists most extinctions enabled the fixture of major evolu- likely to overcome this hurdle are discouraged tionary innovations to which species radiations from working on Lepidoptera because of the anti‐ are commonly attributed. We also do not know intellectual stigma associated with aesthetically how such extinctions may have set the stage for pleasing insects. rapid diversification within groups already Notwithstanding the observations of equipped with the underlying mechanics for Kristensen et al. (2007), it should be acknowl- adaptation. Regardless of our ability to pinpoint edged that the difficulty encountered in generat- such origins, it is possible to identify the relative ing robustly supported hypotheses of relationship order of events, even if rapid diversification of among lepidopteran superfamilies has likely many dominant life forms occurred simultane- been amplified by the fact that much of lepidop- ously. For this reason, molecular data have been teran evolution took place rapidly; many of the looked to as potential saviors of lepidopteran phy- primary events were compressed, and major logeny re-construction. And although they groups might have arisen rapidly and diversified remain promising, methods of temporal dating simultaneously. Most lepidopteran superfami- has proven frustrating, and classifications based lies are thought to have originated in the exclusively on molecular phylogenetic evidence Cretaceous, well before the extinction event that remain suspect as long as clear morphological triggered the end of the Mesozoic Era roughly characters cannot be adduced to support them. 66 mya. However, many of the major macrohet- eroceran (macrolepidopteran) superfamilies are thought to have arisen close to this mark, either 13.5 General Overview in the upper stages of the Cretaceous Period or in the lower Tertiary, and most have undergone The considerable progress in elucidating higher‐ radiations in the past 60 million years, parallel- level relationships – establishing robust support ing those of major flowering plant groups. for some of the major clades and identifying Latitudinal migration of land masses, changes in problematic “wild card” taxa as priorities for atmospheric gas concentrations, and periodic future research – has also incurred equally con- ice ages are likely to have brought about shifts in siderable taxonomic flux within and among lepidopteran diapause that coincided with superfamilies. This flux is likely to continue as changes in the availability of food plants, creat- the higher‐level phylogenetic arrangement ing phenological filters. Certain species radia- remains unstable in several key areas. Few major tions might not have been simply precipitated by groups of Lepidoptera have enjoyed simultaneous­ 13 Diversity and Significance of Lepidoptera 469 stability in rank, composition, and higher‐level usage and been replaced by “,” assignment (e.g., to a superfamily or infraorder). reflecting the removal of butterflies. One large Most lepidopteran families and superfamilies superfamily, the Pyraloidea, remains termino- described in the past 25 years, as well as major logically or colloquially orphaned in this scheme, changes in rank, are scattered throughout the considered neither macrolepidopteran (except by order. The composition and rank of groups some microlepidopterists) nor microlepidop- within the have been the least sta- teran (except by some macrolepidopterists). ble of all the superfamilies. Notwithstanding the Although the composition of Macroheterocera composition of the (butterflies has been ambiguous with respect to other groups and their relatives), flux in the recognition of (e.g., , Doidae, and ), it rank within the Macroheterocera has seems to have stabilized (Regier et al. 2013; been most pronounced within the Noctuoidea. Table 13.1). To summarize matters effectively, it is neces- The more well‐supported traditional group- sary first to clarify some terminology surround- ings of Lepidoptera have corresponded to con- ing the classification of large and small moths, spicuous but not necessarily unreversed butterflies, and skippers. Primary divisions in morphological features. To the extent that our traditional, pre‐Hennigian classification schemes understanding of these features has been refined, differentiated butterflies from everything else, they continued to form the foundation for lepi- recognizing Rhopalocera (butterflies and skip- dopteran classification. Major morphological pers, bearing clubbed antennae) and paraphyletic innovations that we interpret as uniquely derived Heterocera (moths, bearing varied antennal correspond to synapomorphies for a series of morphologies). These reflect popular conven- subordinal, infraordinal, and rankless clade tions used to tell brightly colored day‐flying ani- names applied to nested, progressively less‐ mals from more drab, nocturnal ones. Most of inclusive groups of one or more superfamilies these shortcuts have numerous exceptions and (Fig. 13.1, Table 13.1). Many of the major mor- oversimplify the fundamental diversity in each of phological innovations are associated with adult these groupings. Within Heterocera, a cascade of and larval feeding habits (morphology of the additional groupings existed based on important haustellum or , and endophytophagy but imperfect characters such as wing coupling versus external feeding in larvae); wing venation (Jugatae versus Frenatae), wing venation (primitively homoneurous, or identical in con- ( versus ), separation of figuration between fore‐ and hindwings versus the gonopore from the copulatory orifice the more derived heteroneurous condition); ( versus ), and, most loosely, wing‐coupling mechanisms (e.g., the presence of size ( versus ). forewing jugum in homoneurous moths versus Such classifications persisted long after they were retinaculo‐frenate mechanisms in higher recognized as unnatural. By convention, Lepidoptera); the mechanics of the reproductive “Microlepidoptera” refers to roughly 75% of the system; and, within higher Lepidoptera, the con- moth families, including all the primitive super- figuration of tympanal ears. Many of the gross families. The prefixes “macro” and “micro” are anatomical novelties occurred early in the evolu- especially confusing misnomers, given the exist- tion of the order: the evolution of the haustellum ence of large (e.g., ) moths within the in the glossatan superfamilies from mandibulate primitive superfamilies traditionally thought of ancestors; of modified wing scales in the ances- as micros and the diversity of small moths (e.g., tral and the musculated haustellum Micronoctuinae) in multiple superfamilies of preceding innovations associated with differen- higher Ditrysia. Because the placement of butter- tiated flight mechanics and wing‐coupling flies has remained unstable, the term mechanisms in the Heteroneura; and the mas- “Macrolepidoptera” has gradually fallen out of sive radiation accompanying the origin of the 470 Insect Biodiversity: Science and Society

Table 13.1 Classification of the Lepidoptera.

Order LEPIDOPTERA Linnaeus, 1758 No. of genera No. of spp.

Suborder ZEUGLOPTERA Chapman, 1917 (1 superfamily) 1 Micropterigoidea Herrich‐Schäffer, 1855 (265 spp.) 1 Herrich‐Schäffer, 1855 21 265

Suborder AGLOSSATA Speidel, 1977 (1 superfamily) 2 Agathiphagoidea Kristensen, 1967 (2 spp.) 2 Agathiphagidae Kristensen, 1967 1 2

Clade ANGIOSPERMIVORA Regier et al., 2015 Suborder HETEROBATHMIINA Kristensen & Nielsen, 1983 (1 superfamily) 3 Heterobathmioidea Kristensen & Nielsen, 1979 (10 spp.) 3 Heterobathmiidae Kristensen & Nielsen, 1979 1 10

Suborder Fabricius, 1775 (6 infraorders, all following) Infraorder DACNONYPHA Hinton, 1946 (1 superfamily) 4 Eriocranioidea Rebel, 1901 (30 spp.) 4 Rebel, 1901 5 30

Clade COELOLEPIDA Nielsen & Kristensen, 1996 (5 infraorders, all following) — Superfamily unassigned (1 spp.) 5 Aenigmatineidae Kristensen & Edwards, 2015 1 1 Infraorder ACANTHOCTESIA Minet, 2002 (1 superfamily) 5 Acanthopteroctetoidea* Davis, 1978 (5 spp.) 6 Davis, 1978 2 5 Infraorder LOPHOCORONINA Common, 1990 (1 superfamily) 6 Lophocoronoidea* Common, 1973 (6 spp.) 7 Lophocoronidae Common, 1973 1 6

Clade * Kristensen & Nielsen, 1981 (3 infraorders, all following) Infraorder NEOPSEUSTINA Davis & Nielsen, 1980 (1 superfamily) 7 Neopseustoidea Hering, 1925 (14 spp.) 8 Hering, 1925 4 14

Clade * Packard, 1895 (2 infraorders, all following) Infraorder Common, 1975 (2 superfamilies) 11 8 Hepialoidea Stephens, 1829 (666 spp.) 9 Mnesarchaeidae Eyer, 1924 1 14 10 Stephens, 1829 69 652 13 Diversity and Significance of Lepidoptera 471

Table 13.1 (Continued)

Order LEPIDOPTERA Linnaeus, 1758 No. of genera No. of spp.

Infraorder HETERONEURA Tillyard, 1918 (34 superfamilies, all following) Clade NEPTICULINA Meyrick, 1928 9 Stainton, 1854 (1,046 spp.) 11 Stainton, 1854 13 852 12 Meyrick, 1893 7 194

Clade EULEPIDOPTERA Kiriakoff, 1948 Clade INCURVARIINA Börner, 1939 10 Andesianoidea Davis & Gentili, 2003 (3 spp.) 13 Andesianidae Davis & Gentili, 2003 1 3 11 Bruand, 1850 (583 spp.) 14 Heinemann & Wocke, 1876 12 124 15 Bruand, 1850 5 294 16 Spuler, 1898 11 51 17 Bréthes, 1916 5 16 18 Prodoxidae Riley, 1881 9 97 19 Tridentaformidae Davis, 2015 1 1

Clade EUHETERONEURA Regier et al., 2015 Clade ETIMONOTRYSIA* Minet, 1984 12 Palaephatoidea Davis, 1986 (57 spp.) 20 Davis, 1986 7 57 13 Spuler, 1898 (112 spp.) 21 Tischeriidae Spuler, 1898 3 112

Clade DITRYSIA Börner 1925 — Superfamily unassigned (104 spp.) — Family unassigned (25 genera, 100 spp.) 25 100 22 Millieriidae Heppner, 1982 3 4 14 Latreille, 1810 (3,719 spp.) 23 Spuler, 1898 6 80 24 Psychidae Boisduval, 1829 211 1,246 25 Latreille, 1810 321 2,110 26 Meessiidae (Capuse, 1966) 35 248 27 Dryadaulidae Bradley, 1966 1 35 15 Stainton, 1854 (2205 spp.) 28 Bruand, 1850 13 53

(Continued) 472 Insect Biodiversity: Science and Society

Table 13.1 (Continued)

Order LEPIDOPTERA Linnaeus, 1758 No. of genera No. of spp.

29 Fracker, 1915 4 297 30 Stainton, 1854 100 1,855 16 Stephens, 1829 (1756 spp.) 31 Yponomeutidae Stephens, 1829 94 362 32 Guenée, 1845 7 163 33 Guenée, 1845 48 150 34 Stainton, 1854 28 535 35 Bruand, 1850 1 157 36 Stainton, 1854 32 204 37 Mosher, 1916 1 52 38 Praydidae Moriuti, 1977 3 47 39 Heinemann & Wocke, 1876 13 69 40 Bedelliidae Meyrick, 1880 1 16 41 Scythropiidae Friese, 1966 1 1

Clade APODITRYSIA Minet, 1983 — Superfamily unassigned (1 family, 29 spp.) 42 Heinemann & Wocke, 1876 2 29 17 Simaethistoidea Minet, 1991 (4 spp.) 43 Simaethistidae Minet, 1991 2 4 18 Gelechioidea Stainton, 1854 (18769 spp.) 44 Le Marchand, 1947 72 650 45 Le Marchand, 1947 100 1,200 46 Xyloryctidae Meyrick, 1890 60 524 47 Bruand, 1850 313 3,400 48 (Meyrick, 1883) 114 2,300 49 Heinemann & Wocke, 1876 135 1,792 50 Stainton, 1854 507 4,700 51 Bruand, 1850 47 901 52 Bruand, 1850 5 1,400 53 Heinemann & Wocke, 1876 10 99 54 Rebel, 1901 30 669 55 Meyrick, 1894 24 430 56 Janse, 1917 44 408 57 Herrich‐Schäffer, 1857 6 115 58 Meyrick, 1918 2 30 59 Herrich‐Schäffer, 1857 3 150 60 Schistonoeidae Hodges, 1998 1 1 13 Diversity and Significance of Lepidoptera 473

Table 13.1 (Continued)

Order LEPIDOPTERA Linnaeus, 1758 No. of genera No. of spp.

19 Leach, 1815 (235 spp.) 61 Tineodidae Meyrick, 1885 12 19 62 Alucitidae Leach, 1815 9 216 20 Pterophoroidea Latreille, 1802 (1,318 spp.) 63 Latreille, 1802 90 1,318 21 Carposinoidea Walsingham, 1897 (326 spp.) 64 Meyrick, 1905 9 43 65 Walsingham, 1897 19 283 22 Schreckensteinioidea Fletcher, 1929 (8 spp.) 66 Fletcher, 1929 2 8 23 Epermenioidea Spuler, 1910 (126 spp.) 67 Spuler, 1910 10 126 24 Kyrki, 1988 (66 spp.) 68 Kyrki, 1988 3 66 25 Immoidea Common, 1979 (245 spp.) 69 Common, 1979 6 245 26 Choreutoidea Stainton, 1858 (406 spp.) 70 Stainton, 1858 18 406 27 Galacticoidea Minet, 1986 (19 spp.) 71 Minet, 1986 3 19 28 Tortricoidea Latreille, 1802 (10,387 spp.) 72 Family Tortricidae Latreille, 1802 1,071 10,387 29 Leach, 1815 (2,881 spp.) 73 Agenjo, 1966 14 137 74 Leach, 1815 151 971 75 Dudgeoneidae Berger, 1958 6 57 76 Strand, 1909 18 196 77 Ratardidae Hampson, 1898 3 10 78 Boisduval, 1828 34 113 79 Boisduval, 1828 154 1,397 30 Latreille, 1809 (3,296 spp.) 80 Dyar, 1903 9 32 81 Cyclotornidae Meyrick, 1912 1 5 82 Rambur, 1866 1 10 83 Heppner, 1995 8 120 84 Phaudidae Kirby, 1892 3 15 85 Dyar, 1898 11 80 (Continued) 474 Insect Biodiversity: Science and Society

Table 13.1 (Continued)

Order LEPIDOPTERA Linnaeus, 1758 No. of genera No. of spp.

86 Duponchel, 1845 301 1,672 87 Megalopygidae Herrich‐Schäffer, 1855 23 232 88 Aididae Schaus, 1906 2 6 89 Somabrachyidae Hampson, 1920 4 8 90 Himantopteridae Rogenhofer, 1884 11 80 91 Latreille, 1809 170 1,036

Clade Minet, 1986 31 Whalleyanoidea Minet, 1991 (2 spp.) 92 Whalleyanidae Minet, 1991 1 2 32 Thyridoidea Herrich‐Schäffer, 1846 (940 spp.) 93 Herrich‐Schäffer, 1846 93 940 33 Hyblaeoidea Hampson, 1903 (18 spp.) 94 Hampson, 1903 2 18 95 Prodidactidae Epstein & Brown, 2003 1 1 34 Calliduloidea Moore, 1877 (49 spp.) 96 Moore, 1877 7 49 35 Papilionoidea Latreille, 1802 (18,768 spp.) 97 Papilionidae Latreille, 1802 32 570 98 Hedylidae Guenée, 1858 1 36 99 Hesperiidae Latreille, 1809 570 4,113 100 Swainson, 1820 91 1,164 101 Grote, 1895 (1827) 146 1,532 102 Leach, 1815 416 5,201 103 Nymphalidae Rafinesque, 1815 559 6,152 36 Pyraloidea Latreille, 1809 (15,587 spp.) 104 Latreille, 1809 1,056 5,921 105 Latreille, 1810 1,018 9,666

Clade MACROHETEROCERA Chapman, 1893 37 Mimallonoidea Burmeister, 1878 (194 spp.) 106 Mimallonidae Burmeister, 1878 27 194 38 Drepanoidea Boisduval, 1828 (672 spp.) 107 Chrétien, 1916 2 6 108 Doidae Donahue & Brown, 1987 2 6 109 Boisduval, 1828 122 660 39 Harris, 1841 (1,952 spp.) 110 Harris, 1841 224 1,952 13 Diversity and Significance of Lepidoptera 475

Table 13.1 (Continued)

Order LEPIDOPTERA Linnaeus, 1758 No. of genera No. of spp.

40 Latreille, 1802 (4,723 spp.) 111 Neumoegen & Dyar, 1894 10 145 112 Swinhoe, 1892 53 339 113 Swinhoe, 1892 7 65 114 Phiditiidae Minet, 1994 4 23 115 Turner, 1904 9 94 116 Carthaeidae Common, 1966 1 1 117 Boisduval, 1828 12 59 118 Latreille, 1802 26 185 119 Boisduval, 1837 169 2,349 120 Latreille, 1802 206 1,463 41 Leach, 1815 (23,749 spp.) 121 Swinhoe, 1892 9 20 122 Sematuridae Guenée,1858 6 40 123 Leach, 1815 90 686 124 Geometridae Leach, 1815 2,002 23,002 125 Pseudobistonidae Minet, Rajaei & Stüning 2015 1 1 42 Noctuoidea Latreille, 1809 (42,407 spp.) 126 Miller, 1991 4 8 127 Notodontidae Stephens, 1829 704 3,800 128 Erebidae Leach, 1815 1,760 24,569 129 Grote, 1882 29 520 130 Bruand, 1847 186 1,738 131 Noctuidae Latreille, 1809 1,089 11,772 Total 15,414 157,761

Superfamilies (42) and families (131) are numbered in bold and shaded italics, respectively. Estimates of described species and genera follow those of Nieukerken et al. (2011), variously updated from Sohn et al. (2013, Yponomeutoidea), Heikkilä et al. (2014, Gelechioidea), and Regier et al. (2012, Pyraloidea; 2013, Ditrysia; 2014, Tineoidea; 2015, non‐ditrysian superfamilies). The classification presented herein follows that of Nieukerken et al. (2011), excepting the addition of the Angiospermivora as well as certain higher‐level additions and status changes (families newly described, elevated, or synonymized) published more recently. These include the addition of the homoneurous family Aenigmotineidae (Kristensen et al. 2015) and, in the Tineoidea, of Meessiidae and Dryadaulidae, both elevated in Regier et al. 2015); in the Gelechioidea (addition of Depressariidae, redefined by Heikkilä et al. 2014); Adeloidea (addition of Tridentaformidae; Regier et al. 2015); Mnesarchaeoidea (synonymized with Hepialoidea by Regier et al. 2015); Yponomeutoidea (addition of Scythropiidae, elevated by Sohn et al. 2013); and Geometroidea (addition of Pseudobistonidae; Rajaei et al. 2015). Neither the Myoglossata nor the Neolepidoptera are recovered in the analyses of Regier et al. (2015) due to the removal of the Lophocoronoidea from a position to each of these groups to one adjacent to the Exoporia (Hepialoidea) and the relocation of Acanthopteroctetidae (Acanthopteroctetoidea) to within the Neopseustoidea, but we retain their arrangement in this table per Nieukerken et al. (2011) for reference. Asterisks (*) refer specifically to these departures from Regier et al. (2015) and Fig. 13.1, where the placement of Lophocoronoidea reflects Regier et al. (2015) and Acanthopteroctetoidea is retained as a superfamily and sister to the Neopseustoidea. Significant questions remain regarding superfamily assignments of certain (Continued) 476 Insect Biodiversity: Science and Society

Table 13.1 (Continued)

ditrysian families (e.g., of Millieriidae) and family‐level classification, particularly within the Gelechioidea (Heikkilä et al. 2014), and with respect to the composition of Tineoidea, which seems to be paraphyletic with respect to the remaining Ditrysia in recent analyses (Regier et al. 2013, 2015). The composition of the Macroheterocera follows that of Nieukerken et al. (2011) with the addition of the Mimallonoidea, following the results of Mutanen et al. (2010) and Regier et al. (2013). The Prodidactidae were reassigned to the Hyblaeoidea by Kaila et al. (2013), and the placement of this family remains problematic. Classification problems for the Doidae are even more acute: this family was described and treated as a noctuoid but placed within the Drepanoidea by Nieukerken et al. (2011), and was united with the Mimallonidae by Regier et al. (2013). Nonetheless, the Doidae are retained as a family in the Macroheterocera.

ditrysian reproductive system followed by the described or synonymized since 2011. Certain appearance of exophytophagous larvae and adult family‐ and superfamily‐level rearrangements tympanal organs that enabled avoidance and published subsequently to Nieukerken et al. (2011) deterrence of predators. have been incorporated, but not all recently pub- At this writing (November 2015), 42 superfami- lished hypotheses of relationships are accommo- lies and 131 families are recognized, including dated. Those with the most far‐reaching impacts eight families unassigned to superfamily (five early are discussed, including the ongoing rearrange- lepidopterans, one early Ditrysian, and two ment of the Noctuoidea and the most recent dis- Apoditrysian; Table 13.1) and a smattering of cussions over the placement of butterflies unassigned genera. The most recent global compi- (Mutanen et al. 2010, Kawahara and Breinholdt lation of described lepidopteran genera and spe- 2014). Although a detailed treatment of each cies, included in the classification of Nieukerken superfamily is not attempted here, a perfunctory et al. (2011), is used as the basis for discussion treatment of the most diverse or conspicuous below and for the numbers in Table 13.1. These superfamilies is accompanied by selected family do not necessarily reflect species and genera accounts.

Euheteroneura DITRYSIA (154,554)

Palaephatoidea Eulepidoptera “MONO Tischerioidea Heteroneura TR Andesianoidea Y SIA Adeloidea ” Nepticuloidea

Coelolepida Acanthopteroctetoidea Neopseustoidea Glossata Hepialoidea Angiospermivora Lophocoronoidea Eriocranioidea Heterobathmioidea Agathiphagoidea Micropterigoidea

Figure 13.1 Phylogenetic skeleton of basal lepidopteran superfamilies, revised in part following Regier et al. (2015) but retaining Acanthopteroctetoidea and not specifying of Palaephatoidea. (Table 13.1 provides further elaboration). 13 Diversity and Significance of Lepidoptera 477

13.5.1 Primitive Lepidoptera et al. (2011) outside “Myoglossata,” purportedly on the basis of a proboscis (haustellum) with The most phylogenetically basal of the extant lep- intrinsic musculature, but Regier et al. (2015) idopteran superfamilies (Fig. 13.1) retains several relocate the Acanthopteroctetidae within the primitive features, including well‐musculated Neopseustoidea, which previously comprised a mandibles as adults, lacking the fused galeae single small family distributed in Asia, the Indian (haustellum) that unite the rest of the order; a subcontinent, and western . characteristically rough, fuzzy cephalic vestiture Regier et al. (2015) place the Lophocoronidae as of hair‐like scales; and folded, five‐segmented sister to the ­remaining homoneurous superfami- maxillary palpi (Kristensen 1999a). These basal lies, the Mnesarchaeoidea and Hepialoidea, groups comprise three superfamilies, each which they synonymized under the latter name. assigned its own suborder and each containing a These were traditionally assigned their own sub- single family, the most speciose of which is the order (Exoporia), united by the uniquely config- Micropterigidae. The most derived of these ured female reproductive system. Female superfamilies (Heterobathmioidea) is united with exoporians (hepialoids) have a separate gonopore the remaining Lepidoptera under the name and copulatory orifice, as do the ditrysian Angiospermivora by Regier et al. (2015). Lepidoptera, but lack an internal ductus semi- The glossatan superfamilies, almost 99.9% of the nalis. Spermatozoa deposited in the bursa copul- order, are united by the presence of a coilable haus- atrix during mating travel along an external tellum. Primitive glossatans form a grade of six seminal groove between the ostium bursae and superfamilies with homoneurous wing venation­ the ovipore for fertilization (Scoble 1992, and wing‐coupling mechanisms involving jugal Kristensen 1999b). The family Mnesarchaeidae lobes. The most basal of these is the Eriocranioidea, contains fewer than 10 species, all endemic to the second most diverse of the homoneurous ; the far more diverse and superfamilies; its only family, Eriocraniidae, is ­conspicuous exoporians are the Hepialoidea, Holarctic, with about 30 species characterized by four of whose component families their small size and metallic‐colored wings. (Palaeosetidae, Prototheoridae, Neothoridae, Eriocraniids have micro‐trichiated wing surfaces and Anomosetidae) were synonymized by Regier and, along with the Acanthopteroctetoidea and et al. (2015) under the Hepialidae, or ghost the Lophocoronoidea, have haustella that lack moths, which now contains more than 660 spe- intrinsic musculature. The Acanthopteroctetoidea cies. Hepialids are internal feeders of woody contain a single family, Acanthopteroctetidae, with plants with drastically reduced adult mouthparts; five species restricted to western North America. their centers of known diversity are Australia and Similarly, the Lophocoronoidea contain one family, the Neotropics. They include some of the largest Lophocoronidae, and all six of its species are found “microlepidoptera.” Exoporians form the basal in Australia. These two superfamilies have been branch and only homoneurous clade of the grouped with the remaining Lepidoptera under the Neolepidoptera, a group putatively characterized infraordinal name Coelolepida on the basis of hol- by crochet‐bearing larval prolegs and adecti- low wing scales (Fig. 13.1; Kristensen 1999b). tious, obtect pupae. However, the exporians were Neither of the remaining named primary not admitted by the arrangement of Regier et al. clades within the homoneurous moths, (2015) on grounds of their paraphyletic inclusion Myoglossata or Neolepidoptera, has withstood of the Lophocoronoidea. recent tests of monophyly by Regier et al. (2015) The heteroneurous “Neolepidoptera” or based on the placement of Acanthopteroctetidae Heteroneura are united by numerous features, and the Lophocoronidae in more derived posi- including their wing venation, retinaculo‐frenate tions within the tree (Fig. 13.1; cf. Table 13.1). mechanism of wing coupling, and loss of the first Both families had been placed by Nieukerken abdominal sternum (Davis 1999). 478 Insect Biodiversity: Science and Society

Phylogenetically, the Heteroneura (as well as the 13.5.2 Ditrysia Eulepidoptea and Euheteroneura, all subtended The Ditrysia are characterized by a uniquely by a common node) straddle the monotrysian derived female reproductive system in which a and ditrysian superfamilies; the heteroneur- separate gonopore and copulatory orifice are ous monotrysians span the paraphyletic grade linked internally via the ductus seminalis (as ­comprising the Nepticuloidea, the cosmopolitan opposed to externally, as in the exoporian con- Adeloidea (~584 species), the monobasic figuration) (Fig. 13.2). The Ditrysia include the Andesianoidea endemic to Andean South traditional “Macrolepidoptera” and, with the America, and the ambiguously related exception of the Nepticuloidea, they include all Tischerioidea (trumpet moths, 110 species) and of the superfamilies that have more than 1000 Palaephatoidea (57 species). These groups are described species. The number (14) of major dit- referred to as the monotrysian heteroneura rysian superfamilies with more than 1000 spe- because they retain a single opening for copula- cies nearly matches the number of minor ones. tion and oviposition (Davis 1999). Nepticuloids, Twenty families grouped into three diverse the most basal heteroneurans, include the small- superfamilies – Tineoidea, Gracillarioidea, and est lepidopterans, some with forewing lengths of Yponomeutoidea – represent the primitive 1.5 mm. The composite families of the Adeloidea Ditrysia. One primitive ditrysian family, the have undergone some nomenclatural flux with Millieriidae, is currently unplaced. the inversion of the nominotypical superfamily name from Incurvarioidea. They are, in decreas- 13.5.2.1 Tineoidea ing order of species richness, the fairy longhorn The most diverse of the primitive ditrysian moths (Adelidae, ~294 species), the Heliozelidae superfamilies includes the bagworms (123 species), the yucca moths (Prodoxidae, ~98 (Psychidae, ~1350 species), a cosmopolitan but species), the Incurvariidae (~51 species), the primarily Old World group (Davis and Robinson Cecidosiidae (16 species), and the recently 1999); the moths and clothes moths in described monobasic Tridentaformidae. In the the cosmopolitan Tineidae (~2110 species); and configuration of Regier et al. (2015), the Adeloidea the minor Old World family Eriocottidae (~80 and Andesianoidea represent the most basal species). Recent attention has resulted in the branch of the Eulepidoptera, characterized in elevation of two tineid subfamilies to family sta- part by the presence of pilifers and precisely cou- tus, the primarily Holarctic Meessiidae (248 pled galeae (haustellum). The Palaephatidae, species) and the cosmopolitan Dryadaulidae which exhibit a Gondwanan ­distribution (i.e., (Regier et al. 2015); and the description of a new South America, Australia, and southern ), monobasic family, the Aenigmatineidae from and the widespread Tischeriidae represent the Australia (Kristensen et al. 2015). Other recent most likely candidates for the sister group of the arrangements have reduced the New World Ditrysia (Davis 1999, Wiegmann et al. 2002), family to subfamily status with which they are united under the name (Acrolophinae) within the Tineidae (Regier Euheteroneura by Regier et al. (2015). In contra- et al. 2014). Adult tineoids are generally recog- diction with morphological evidence, Regier nizable by virtue of dark bristles on the labial et al. (2015) obtained results suggesting poly- palpi; short, disassociated galeae; and erect phyly of the Palaephatoidea, with South American scales on the frons. Most females bear a pair of Palaephatus sister to the Ditrysia and the couplet ventral abdominal pseudapophyses on A10. The of Australian palaephatid genera Azaleodes and bagworms (Psychidae) are known for their ten- Ptyssoptera sister to the Tischerioidea, but they dency toward female neoteny, in the most refrained from altering the classification pending extreme cases resulting in pupal mating, and further analyses. several other features correlated with eruptive 13 Diversity and Significance of Lepidoptera 479

Noctuoidea MACROHETEROCERA Lasiocampoidea Bombycoidea Geometroidea Drepanoidea Mimallonoidea OBTECTOMERA Pyraloidea Papilionoidea Pterophoroidea Carposinoidea Epermenioidea Alucitoidea Calliduloidea Hyblaeoidea Thyridoidea Gelechioidea Zygaenoidea Cossoidea Tortricoidea Galacticoidea APODITRYSIA Immoidea Choreutoidea Schreckensteinioidea Urodoidea Yponomeutoidea Gracillarioidea

Tineoidea

Figure 13.2 Reduction of Regier et al. (2013: figure 3), modified in part by retaining usage of Nieukerken et al. (2011) of Carposinoidea in place of Copromorphoidea. The paraphyly of Tineoidea and the polyphyly of Carposinoidea (= Copromorphoidea) and Palaephatoidea obtained in analyses of Regier et al. (2013, 2015) are not reflected; as in those studies, Whalleyanoidea and Simaethistoidea are not included. or outbreak species, high fecundity, dispersal exhibiting conspicuously autapomorphic fea- via larval ballooning on silken threads, and pol- tures before reverting to more eruciform or cat- yphagous feeding habits (Rainds et al. 2009). erpillar‐like forms in later stages. Gracillarioid pupae are characteristically extruded from the 13.5.2.2 Gracillarioidea cocoon prior to eclosion, and adults bear spines The gracillarioids represent a significant radia- on the abdominal terga and a smoothly scaled tion of more than 2000 described species of frons (Davis and Robinson 1999). Most of the small moths whose larvae are miners of species richness in this group is concentrated in and grasses and can be of significant economic one worldwide family, the Gracillariidae, with importance. Many gracillariid larvae are hyper- more than 100 genera and 1800 described spe- metamorphic, with early sap‐feeding instars cies. This group is in considerable need of study. 480 Insect Biodiversity: Science and Society

13.5.2.3 Yponomeutoidea the gelechioids remain undescribed is accurate, In counterpoint to the gracillarioids, this cosmo- then the Gelechioidea might be the largest lepi- politan superfamily of more than 1756 described dopteran superfamily. The largest families are species represents the earliest major radiation of the Gelechiidae (~4700 species), Oeco­phor­idae moths with externally feeding larvae, distributed (3308), Elachistidae (~3201), Cosmo­pterig­idae among 11 recognized families, including the (1792), Coleophor­ ­idae (1386), and Lecitho­ recently elevated Scythropiidae (Sohn et al. 2013, ceridae (~1200); the remaining 11 families con- Lewis et al. 2015). The largest of these are the tain under 1000 described species each. Adult Glyphipterigidae or sedge moths (~535 species), gelechioids can be identified by a combination of Yponomeutidae or ermine moths (~363 species), characters, first and foremost the overlapping and Lyonetiidae (~204 species). Among the scales on the basal half of the haustellum. smaller families is the commonly encountered and Because at least two unrelated groups (Pyraloidea brightly colored Attevidae (webworms, ~50 spe- and Choreutoidea) possess a similar feature, the cies). The Plutellidae (~150 species) include web‐ gelechioids can be differentiated by the absence building leaf skeletonizers, such as the of tympanal organs (present in pyraloids) and diamondback moth Plutella xylostella L., which the absence of small, naked, partially segmented are pests of brassicaceous crops. Adult male maxillary palps (present in choreutids). Other yponomeutoids are usually diagnosed by unique gelechioid features include a smoothly scaled pleural lobes surrounding the genitalia (Dugdale head and four‐segmented maxillary palpi folded et al. 1999a). and parallel with the base of the haustellum, and characteristically upturned and with an elon- 13.5.3 Apoditrysia gated third segment (Hodges 1999). Gelechioid larvae can be identified in part by the location of The remaining 26 ditrysian superfamilies make the subdorsal pinaculum above the spiracle on up the Apoditrysia. The so‐called higher Ditrysia A8; in the Tortricidae the pinaculum usually is are characterized by shortened apodemes with anterior to the spiracle. enlarged bases on sternum II (Minet 1991). All of the most diverse gelechioid families and A phyletic grade of pre‐obtectomeran apoditry- almost all the minor families are worldwide in sians is made up of 14 superfamilies domi- distribution, with various centers of diversity. nated by Gelechioidea (~18,489 species) and The Gelechiidae (twirler moths, ~4700 species) Torticoidea (~10,387 species), followed in order represent the largest, most economically impor- of decreasing species richness by the Zygaenoidea tant, and least comprehensively studied of the (~3296 species), Cossoidea (~2881 species), and gelechioid families. Gelechiids are small moths Pterophoroidea (~1318 species); the remaining with endophagous larvae identifiable in part by nine superfamilies each contain fewer than 500 the colinear abdominal setae on A9. described species. The composition of the The Oecophoridae (concealer moths, ~3308 Apoditrysia remains controversial, in that the species) have a center of species richness in large superfamily Gelechioidea is ambiguously Australia, and include a number of economi- placed (Kaila 2004). cally important pests of stored grains, textiles, and various palms (), as well as would‐ 13.5.3.1 Gelechioidea be biocontrol agents. The Elachistidae (grass The most diverse of the microlepidopterans, the miners, ~3201 species) represent an important Gelechioidea, as currently circumscribed, group of graminivorous insects with several fos- includes more than 18,000 described species dis- sil genera described from Baltic Amber; adults tributed in 17 families, the rank and classifica- are usually identified by their characteristically tion of which have been highly unstable. If the upturned feather‐like forewing fringe. The estimate of Hodges (1999) that more than 70% of Cosmopterigidae (~1792 species) are a family of 13 Diversity and Significance of Lepidoptera 481 small, ­narrow‐winged moths concentrated in highest taxonomic concentration of fruit and nut the Australian region, with larvae that feed pests in the Lepidoptera. The most well‐known of internally on various parts of their food plants. these pests include the codling moth pomo- They also include aquatic species, as in the nella, the light brown apple moth Epiphyas post- Hawaiian endemic Hyposmocoma (Schmitz and vittana, the European grapevine moth Lobesia Rubinoff 2011). The Coleophoridae (case‐bear- botrana, and spruce budworms (Choristoneura ers, ~1386 species) are concentrated in the spp.). The potential economic impacts of tortric- Holarctic. Adult coleophorids are typically rec- ids are as far‐reaching as the diversity of their food ognized by their visibly fringed wing margins; plants, threatening markets as varied as avocado, their larvae, as the name suggests, feed from the orange juice, and wine production. Adult tortric- safety of silken cases following their early instars ids are united by characteristic flat ovipositor as internal feeders. Behaviors associated with lobes in the female genitalia (Horak 1999), but can case‐building and the morphology and architec- be identified by a combination of characters that ture of the cases have been the focus of phyloge- include an unscaled proboscis, rough‐scale head, netic research (Bucheli et al. 2002), paralleling porrect or horizontal three‐segmented labial palpi analogous studies of cocoon‐ and case‐building with a characteristically short apical segment, in caddisflies (Weaver and Morse 1986, Wiggins reduced maxillary palpi, and the presence of ocelli and Wichard 1989, Stuart and Currie 2001). The and chaetosemata (Horak 2006). Tortricid larvae Lecithoceridae (long‐horned moths, ~1200 spe- are varied in their feeding habits, ranging from leaf cies) are concentrated in the Australian and rollers, ‐ and litter‐feeders, and gall‐makers Oriental regions, and can be recognized from to borers of , fruits, and seeds. They are read- other gelechioid families by their long antennae ily identified by the presence of a common pinacu- and reduced or absent gnathos in the male geni- lum or saddle on A9 and the characteristic talia (Park 2011). configurations of the secondary dorsal pinacula in each of the two major subfamilies, Tortricinae and 13.5.3.2 Pterophoroidea Olethreutinae. These taxa overlap in their areas of Of the remaining four most diverse pre‐ concentration: the Australasian, Neotropical, and Obtectomeran Apoditrysia, the Pterophoroidea Palearctic regions for the Tortricinae versus the or plume moths are the smallest, containing a Nearctic, Palearctic, and Oriental regions for the single cosmopolitan family, the Pterophoridae Olethreutinae (Heppner 1991). (~1318 species), noteworthy for their highly modified, characteristically divided wings, 13.5.3.4 Cossoidea extremely long legs, and unique appearance at The carpenter moths (Cossidae, ~971 species), rest. Pterophorids include several important clear‐winged moths (Sesiidae, ~1397 species; for- pests of ornamental plants and numerous spe- merly recognized as its own superfamily cies used in biocontrol of invasive plant species. ), and giant butterfly moths (Castniidae, 113 species) include the most massive of the 13.5.3.3 Tortricoidea ­ditrysian ‘microlepidoptera’; they are stem‐ and Notwithstanding the enigmatic Heliocosma wood borers with many of the features commonly (placed its own family, the Heliocosmidae, by associated with such habits, including grub‐like Regier et al. 2013), this superfamily comprises a coloration and motile pupae that facilitate adult single highly diverse and widespread family, the eclosion. Sesiids are almost all diurnal and rarely Tortricidae, with more than 10,300 described spe- collected, except through rearing or pheromone‐ cies grouped in three subfamilies. The Tortricoidea trapping efforts. The Castniidae, or giant butter- include more than 700 species of economically fly‐moths, are likewise diurnal and are implicated important pests, representing the highest concen- in mimetic complexes involving a range of but- tration in any microlepidopteran family and the terflies and other moths. 482 Insect Biodiversity: Science and Society

13.5.3.5 Zygaenoidea (Scoble 1986, Weintraub and Miller 1987). The The 12 currently recognized zygaenoid families link with hedylids was controversial when intro- are perhaps more diverse behaviorally and mor- duced, as it seemed to imply potential derivation phologically than their taxonomy suggests. of butterflies from Geometroidea, which would They include the only two lepidopteran families in that case have been rendered paraphyletic. (Epipyropidae and Cyclotornidae) with ectopara- The monophyly of the “Hesperioidea” was not in sitic larvae, their hosts being fulgoroid planthop- question; the discussion was primarily one of pers, leafhoppers, and scale insects. Many placement and thereby rank. Here the simplified zygaenoids are chemically defended as larvae higher classification of Nieukerken et al. (2011) is (e.g., Dalceridae, Megalopygidae, and followed, in which both the skippers (Hesperiidae) Limacodidae), and the most diverse zygaenoid and the “moth‐butterflies” (Hedylidae) accom- family, the Limacodidae (slug caterpillars, ~1672 pany the five true butterfly families within the species), are as fascinating for their unique larval Papilionoidea instead of forming their own epon- locomotory mechanism (Epstein 1995) and strik- ymous superfamilies. This arrangement is con- ing appearance as for their urticating spines. As sistent with the phylogenetic analysis of Heikkila in the related Cossoidea, at least one major diur- et al. (2012), who combined morphological char- nal lineage within the Zygaenidae (~1036 spe- acters with sequence data from eight gene regions cies) has been accompanied by chemical to recover [Papilionidae + [[Hedylidae + Hesperi sequestration of pyrrolizidine alkaloids, apose- idae] + [Pieridae + [Nymphalidae + [Riodinidae matism, and mimicry. The phyletic breadth of + Lycaenidae]]]]. Their results suggested an butterflies and moths associated with the early Cretaceous origin for the butterflies sensu Zygaenidae via Müllerian mimicry rings in Asia lato, with diversification accelerating post‐ alone is perhaps greater than that associated with Cretaceous–Paleogene. The exclusively any other lepidopteran family. Neotropical Hedylidae, with fewer than 40 described species, is the smallest of these, united 13.5.4 Obtectomera in part by the reduced foreleg and characteristic adult resting posture with midlegs raised (cf. Although supported by recent molecular work, Thyrididae). The diverse and cosmopolitan this grouping rests on weakly corroborated mor- Hesperiidae, with more than 4000 described spe- phological grounds. It includes all Apoditrysia cies, is most diverse in the tropics and includes with the first four pupal abdominal segments one of the largest assemblages of lepidopterous immobile and the pulvillus in the adult pretarsus insects associated with grasses and other com- modified with a dorsal lobe (Minet 1991). melinids, the subfamily Hesperiinae, or grass Historically, these included the “pyraloid grade” skippers. Skippers are strong flyers and, with of six superfamilies and the much larger exceptions, typically drab in coloration. They Macrolepidoptera (Kristensen and Skalski 1999), form an unambiguously supported monophyl- but these loose groups have largely dissolved, as etic group, united by the wide separation of will be summarized following individual super- antennal bases, characteristically hooked anten- family treatments. nae, and a narrow hind wing cell formed by the The phylogenetic position of the most conspic- union of the R and Sc veins, among other fea- uous diurnal Lepidoptera, the butterflies and tures. caterpillars are usually character- skippers (Papilionoidea), is among the more con- ized by tapering at either end, enhancing the troversial. Several of the component papilionoid appearance of the enlarged head capsules com- families have been recognized as superfamilies. It mon among grass‐feeding Lepidoptera. has been suggested that butterflies represent The true butterflies include, in order of decreas- derived geometroid‐like moths, with the enig- ing size, brush‐footed butterflies (Nymphalidae, matic Hedylidae at the center of this discussion > 6150 species described); the blues, coppers, and 13 Diversity and Significance of Lepidoptera 483 hairstreaks (Lycaenidae, > 5200 species); the of riodinids exhibit a uniquely configured costa. metalmarks (Riodinidae, > 1530 species); sul- Larvae of both families tend to be dorsolaterally phurs (Pieridae, ~1164 species); and the swallow- compressed and have evolved unique, com- tails (Papilionidae, 570 species). Swallowtails, so monly mutualistic associations with ants, which named for the modified hind wings of many spe- they supply with nutrient‐rich secretions in cies, are perhaps most conspicuous of all the but- return for defense against parasitoids (reviewed terflies. Their caterpillars are almost as well by Pierce et al. 2002). Some myrmecophilic rio- known and recognized, in part, by the presence of dinid larvae, the singing caterpillars of DeVries the post‐cephalic repugnatorial gland, the osme- (1990, 1991), produce substrate‐borne sounds terium. Swallowtails include the largest of the to communicate with ants for protection. butterflies, the birdwings () native to the The Nymphalidae include some of the most Indian subcontinent, Southeast Asia, and popular butterflies. Several nymphalids, most Australasia, which are now listed by CITES (the obviously the monarch Danaus plexippus Convention on International Trade in Endangered (Danainae), but also species of the , Species of Wild Fauna and Flora) and thereby such as the red admiral Vanessa atalanta, are heavily restricted or banned from international well‐known seasonal migrants. Nymphalids com- trade. Many papilionids feed as larvae on chemi- prise the most diverse assemblage of butterflies, cally defended hosts, for example, in the both in terms of species richness and in that many Aristolochiaceae and . Having evolved of its at least 12 component subfamilies were, the ability to sequester and coopt defensive com- until relatively recently, considered to be families. pounds such as aristolochic acid from their larval Now included under the umbrella name of brush‐ host plants, birdwings and their relatives repre- footed butterflies are the admirals, fritillaries, sent a textbook example of coevolution (literally, longwings, monarchs, morphos, owls, and as they feature on the cover of Futuyma’s 1986 satyrs – a cosmopolitan cluster reaching its great- edition of Evolutionary Biology). Other butterflies est richness in the Neotropics. Nymphalids are have evolved analogous strategies for exploiting united by a variety of wing venational characters, allelochemicals of their host plants: glucosinolates grooves on the antennal undersides, and with from Brassicales in the case of Pieridae (Edger exceptions reduced or atrophied forelegs in both et al. 2015); cardiac glycosides from milkweeds sexes. Larvae in the Nymphalinae tend to be (Asclepiadaceae) in the case of monarchs and spined. The primary lineages are the snout but- other Danainae (Nymphalidae) (Parsons 1965); terflies (Libytheinae); the milkweed butterflies and cyanogenic glycosides from in the (Danainae), including the clearwing butterflies case of Heliconius (Nymphalidae) (Gilbert 1972). and their relatives (), many of which are Whites and sulphurs (Pieridae) are worldwide involved in Müllerian mimicry rings by virtue of in distribution excepting New Zealand; their larval sequestration of pyrrolizidine alkaloids; the synapomorphies include fully developed fore- ­longwings (Heliconiinae), including Heliconius legs in both sexes (cf. Nymphalidae) and bifid spp., which form the nexus of innumerable stud- tarsal claws, distinguishing them from papilio- ies of mimicry and coevolution; the related, often nids. Pierid pupae are suspended with the aid of mimetic Limenitidinae; the Nymphalinae and a silken girdle secured abdominally rather than related subfamilies, an assemblage with broad thoracically as in the Papilionidae. host associations; and the Satyrinae and their rel- The Riodinidae and Lycaenidae form a closely atives, including the owl butterflies, morphos, related pair of families that are worldwide in and satyrs, which collectively form the largest their distribution, with much of their species radiation of grass‐, sedge‐, and other monocot‐ richness (especially that of the Riodinidae) con- feeding Lepidoptera. Relationships among the centrated in the Neotropics. Adult males in major nymphalid lineages have been studied both families have reduced forelegs; hindwings intensively over the past decade. 484 Insect Biodiversity: Science and Society

Primary among the traditional pyraloid‐grade moths (e.g., elutella and Plodia inter- superfamilies are the Thyridoidea, Hyblaeoidea, punctella), wax moths (e.g., Galleria melonella), and Calliduloidea. Until the recent assignment and the nubilalis. of Prodidactidae to the Hyblaeoidea, each of Considered neither a traditional microlepidop- these superfamilies included a single family of teran nor a true macroheteroceran superfamily, brightly colored, diurnal species. The Thyrididae pyraloid larvae are similar to macroheterocera by are primarily pantropical with a few species in virtue of having two prespiracular setae instead of the Nearctic or Palearctic; they are readily dif- the microlepidopteran three. Adult pyraloids ferentiated by their characteristic wing shape have conspicuous maxillary palpi and, as in the and resting posture (with midlegs raised, as in two large macroheteroceran moth superfamilies, the Hedylidae) (Dugdale 1999b). Like the bilateral ultrasound detection organs. As in the Thyrididae, the less diverse, primarily Old Geometroidea, these organs are abdominal but World Hyblaeidae or teak moths, the primary are thought to have evolved independently, and host plants of which are within the Lamiales, although neither is considered homologous with can be differentiated on the basis of characters the thoracic tympana characteristic of the in the adult legs. Each of these families also has Noctuoidea, Regier et al. (2013) suggested the been included within the Pyraloidea, but as possibility that ultrasound detection in these recent molecular evidence suggests, these place- groups might be attributable to a single evolution- ments are poorly supported and superfamily ary origin near the base of the Macroheterocera. status is warranted. Although the Hyblaeoidea The two component pyraloid families, the and Thyridoidea share unique modifications of Pyralidae and Crambidae, the latter referred to as the larval spinneret, Kaila et al. (2013) declined grass moths, are differentiated as adults by the to propose a sister group relationship of the two configuration of the tympanic organ (Munroe superfamilies in recognition of apparently con- and Solis 1999). In the Crambidae, these organs flicting molecular data. The Callidulidae or but- bear a praecinctorium, and the tympanum and terfly‐moths are found in the Old World, conjunctiva are set at an oblique angle, whereas primarily in the Oriental region, with an the Pyralidae have no praecinctorium and exhibit endemic species in (Minet 1999). a co‐planar arrangement. The Crambidae are the They are united by several features of the male more diverse in terms of species richness (roughly and female genitalia and the adult foreleg. From 9655 versus 5921 in Pyralidae; Nieukerken et al. a phenomenological perspective, it is among the 2011) and number of subfamilies (13 versus five; obtectomerans where we begin to see repeated Regier et al. 2012). The Phycitinae (~3450 spe- origins of bright, aposematic coloration in asso- cies) represent the largest pyralid subfamily, and ciation with adult diurnal activity, the callidulids include roughly two‐thirds of the described pyra- representing a signature example. The precise lids. Taxonomically, the Crambidae are domi- placements of the Immoidea and Carposinoidea nated by the (~3767 species), (Carposinidae and Copromorphidae; formerly (~1987 species), and Copromorphoidea) remain uncertain. (~1450 species) (Regier et al. 2012). Pyraloids are Depending on the final phylogenetic residence noteworthy not only for their diversity of eco- of the Papilionoidea, the Pyraloidea probably rep- nomically important pests of graminaceous crops resent the most diverse of the obtectomeran such as rice, corn, and sugarcane, but also for superfamilies outside the Macroheterocera, their numerous grass‐feeding and wetland‐asso- including more than 16,000 described species, ciated species. The Crambinae make up one of with possibly as many awaiting discovery. the more diverse assemblages of graminivores Pyraloids include the second largest cohort of within the Lepidoptera and include some of the pests (~750 species) of any lepidopteran super- few aquatic and semi‐aquatic lepidopteran larvae, family, including rice borers, flour and meal as well as a number of important biocontrol 13 Diversity and Significance of Lepidoptera 485 agents that are used against invasive wetland altogether: first as sister to a Cossoidea/Sesioidea plants. Pyralids, although less diverse, affect a + Zygaenoidea, rendering Macrolepidoptera, broader range of resources as pests of legumes, Apoditrysia, and Obtectomera all polyphyletic stored grains, flours, cereals, dried fruits, and (Regier et al. 2009); next, as embedded within an managed hives, and as defoliators of culti- assemblage of pyraloid‐grade superfamilies vated pines. They, too, include important biocon- (Calliduloidea, Hyblaeoidea, and Thyridoidea) trol agents, for example, of prickly pear (Opuntia; and pre‐obtectomeran Apoditrysian superfami- Clausen 1978). lies (Pterophoroidea, Alucitoidea, and Eper­ menioidea), collectively forming a sister group to 13.5.5 Macroheterocera the [Pyraloidea +Macroheterocera], all within a monophyletic Obtectomera with the Gelechioidea The remaining superfamilies have demonstrated as the sister taxon (Regier et al. 2013); and most varying degrees of compositional as well as phy- recently as basal within a re‐composed logenetic instability. Neither the pyraloid grade Obtectomera that includes the Gelechioidea as nor the Macroheterocera seems to be stable in its follows: [[Papilionoidea + [[Gelechioidea + [Calli arrangement; different analyses have placed the duloidea + Thyridoidea]] + [Pyraloidea + Carposinoidea and/or the Immoidea basal within [Mimallonoidea + Macroheterocera]]]] (Kawahara the Apoditrysia (Regier et al. 2009; Mutanen and Breinholdt 2014). Mutanen et al. (2010) had et al. 2010), and more recently the Carposinoidea presented similar results, with the Papilionoidea firmly within the Obtectomera (Regier et al. more or less embedded within traditional micro- 2013). The uncertain placement of the lepidopteran groups. Papilionoidea highlights the instability of super- The Bombycoidea include 10 families of large familial relationships, as does the unstable com- moths. The smallest families include the mono- position of the Bombycoidea/Lasiocampoidea typic Carthaeidae as well as the Phiditiidae (23 and placement of the Drepanoidea and species, Old World), Endromidae (59 species, Mimallonoidea relative to the Geometroidea (i.e., Palearctic), Brahmaeidae (65 species, Old World), straddling the base of the Macroheterocera). and Anthelidae (94 species, Australian). The Following the treatments of Regier et al. (2009), remaining five range from the moderately sized which circumscribed Macrolepidoptera to the Apatelodidae (145 species, New World, primarily exclusion of butterflies (Papilionoidea), and Neotropical), Bombycidae (185 species, Old Mutanen et al. (2010), who obtained an expanded World, primarily Oriental), and Eupterotidae (339 Macrolepidoptera that included the butterflies species, Old World) to the large, diverse and cos- and the Pyraloidea as well as related Thyridoidea, mopolitan Sphingidae (1463 species) and Hyblaeoidea, and Calliduloidea, Nieukerken et al. Saturniidae (2349 species), the latter with its (2011) adopted Macroheterocera to the exclusion greatest diversity in the Neotropics. Except for of the butterflies (Papilionoidea) and the sack‐ the worldwide Saturniinae, eight of nine recog- bearers (Mimallonoidea). Subsequent empirical nized saturniid subfamilies are continentally work has retained the Mimallonoidea within the restricted. Macroheterocera (Regier et al. 2013). Both Regier Perhaps with the exception of the silk moth et al. (2013) and Kawahara and Breinholdt (2014) mori, the Saturniidae and the retained the circumscription of the Papilionoidea Sphingidae include the most well‐known and by Nieukerken et al. (2011) to include the skip- popular bombycoids, and are among the most pers (Hesperiidae) and the moth‐butterflies intensively studied. Their respective life histo- (Hedylidae), each of which had been recog- ries have been contrasted by Janzen (1984) and nized as superfamilies. Both Regier et al. (2009, Bernays and Janzen (1988). Saturniids tend to 2013) and Kawahara and Breinholdt (2014) disas- be associated as larvae with the foliage of woody sociated the butterflies from the Pyraloid grade plants and do not feed as adults, bearing reduced 486 Insect Biodiversity: Science and Society

or vestigial mouthparts and exhibiting little ten- farm and garden pests. Because of its size, avail- dency towards long‐distance dispersal. The ability, and ease in rearing, M. sexta has been Hemileucinae are especially well known for used extensively as a model organism in insect their variety of defensive strategies, including physiology and neurobiology laboratories. urticating spines on the larvae, false eyespots on The Lasciocampoidea, the lappet moths and the wings, and aposematic coloration and tent caterpillars, include a single family of nearly behaviors in adults of diurnal species, possibly 2000 species worldwide in their distribution. associated with allelochemicals synthesized de Lasiocampids bear similarities to bombycoids novo. Sphingids, by contrast, tend to specialize in their overall appearance, reduced mouth- on various forbs and vines that bear either parts, and in many cases their size. Because of defensive allelochemicals or volatile compounds their conspicuous aggregations and tent‐form- exploited by female moths as oviposition cues. ing behavior, tent caterpillars ( Sphingids as a group are highly vagile and many spp.) are well‐known pests, especially of orna- are seasonal migrants; their presumably high mental trees, but generally do not kill the plants energetic needs as adults may be met, in part, by on which they feed. Although many lepidopter- means of highly efficient mouthparts. The exist- ans are gregarious as larvae, Malacosoma cater- ence and activity of Xanthopan mor- pillars were the first presocial larvae shown to gani Walker, bearing a proboscis more than use chemical recruitment trails (Fitzgerald and 30 cm long, was predicted by Darwin and Peterson 1983) and have figured more promi- Wallace following examination of the Malagasy nently in the sociobiology literature than any orchid Angraecum sesquipedale Thouars, which other lepidopterans not associated with ants has an unusually long nectar‐bearing spur (Costa 2006; Fitzgerald 1995). unreachable by other insects. Geometroidea and its five component fami- Bombycoids are of economic importance in lies – Epicopeiidae (20 species), Sematuridae (40 various ways. The mopane worm Gonimbrasia species), Uraniidae (686 species), the recently belina constitutes an important source of pro- described monobasic Pseudobistonidae, and the tein for indigenous southern Africans, and a sig- overwhelming Geometridae (> 23,000 spe- nificant industry surrounds its cultivation. The cies) – make up the second most diverse lepidop- cultivation of the silk moth teran superfamily. The Geometroidea combined (Bombycidae) is responsible for sericulture, with the Noctuoidea make up more than 40% of established in China for more than 5000 years. described Lepidoptera species. In addition to the Silk played a role in international commerce loss of abdominal prolegs, a reliable synapomor- long before being smuggled from China to the phy for geometroids is the shape of the larval Byzantine Empire during the 6th century ad. labium, in which the spinneret is shorter than the Bombyx mori is the only known truly prementum along its midline (Minet and Scoble ­domesticated insect, unable to reproduce in the 1999). Like the Pyraloidea, adult geometroids wild. Although saturniids are rarely considered bear tympana on the first abdominal segment, but pests, outbreaks of the orange‐striped oakworm are readily distinguished from pyraloids by the senatoria () in north- unscaled proboscis and usually broad wing shape. eastern North America and the buck moth Although diverse, the internal classification of the Hemileuca maia (Hemileucinae) in southeast- Geometridae is not excessively complicated rela- ern North America have resulted in the local- tive to other comparably sized groups. The most ized defoliation of wild and ornamental , recent work (Sihvonen et al. 2011) essentially sup- respectively. Several sphingid species, most ported the monophyly of the four major subfami- notably the closely related tobacco hornworm lies (, Larentiinae, Sterrhinnae, Manduca sexta and tomato hornworm and ); the remaining four Manduca quinquemaculata, are significant (Oenochrominae, Archiearinae, Desmobathrinae, 13 Diversity and Significance of Lepidoptera 487 and Orthostixinae) have not been as robustly organs whose orientation varies by group. They tested, and three appear to be polyphyletic include the prominent moths (Notodontidae, (Oenochrominae and Desmobathrinae) or, in the 3800 species), the owlets (Noctuidae, ~12,000 case of the Orthostixinae, nested within the species), the tiger moths (~11,000 spe- Ennominae. cies, cosmopolitan with a Neotropical center of Representing the second largest lepidopteran distribution), and the tussock moths family next to the Erebidae, the Geometridae (~2800 species, nearly cosmopolitan but primar- are perhaps most familiar as inchworms, so ily Old World), the latter two formerly recog- named for the loss of larval prolegs on abdomi- nized as families but now grouped along with the nal segments 3–5 (retaining those on A6 and underwings () and other former noctuid A10), which produces their characteristic loop- subfamilies in the Erebidae (~25,000 species). ing gait (enabling rapid movement) and hence The remaining recognized noctuoid families are the appearance of measuring or meting out dis- the Oenosandridae (eight species, endemic to tance. They can be differentiated from superfi- Australia), Euteliidae (520 species, cosmopolitan cially similar loopers in the Noctuidae, which but primarily Afrotropical), and Nolidae (1738 have lost or vestigial prolegs on A3–4, retaining species, cosmopolitan but primarily Old World those on both A5 and A6. Adult geometroids tropics), the latter two of which formerly were can appear butterfly like at rest, and include treated as subfamilies of Noctuidae. Noctuoids many diurnal butterfly mimics. The are characterized by the presence of metatho- Geometridae include few major agricultural racic tympanal organs and their associated pests but several forest pests, including the structures. invasive winter moth Operophtera brumata L. In the past 15 years, the Noctuoidea has under- Several geometrid groups display trends toward gone perhaps the most controversial taxonomic female aptery (winglessness), dispersing pri- rearrangement of any superfamily, precipitated marily through larval ballooning (Edland 1971). by increasing recognition that a large cohort of The geometrid genus Nemoria provided the the Noctuidae bore significant phylogenetic first known example of a tannin‐induced sea- affinities to the then‐recognized Arctiidae (tiger sonal polyphenism, in which larval mimicry of moths) and the Lymantriidae (tussock moths) its host‐plant () catkins is suppressed in late‐ (Mitchell et al. 2000, 2006; Fibiger and Lafontaine season generations when the catkins are no 2005; Lafontaine and Fibiger 2006). Traditionally, longer in flower to aid crypsis (Greene 1989). noctuoid families were demarcated along differ- Each of the remaining families, other than the ences in fore‐ and hindwing venation and the recently described monobasic Pseudobistonidae, configuration of tympanal organs, with the is made up of primarily diurnal species vari- Oenosandridae and Notodontidae considered ously associated with swallowtail butterflies basal with respect to the remaining families on (Papilionidae) in Müllerian mimicry rings. the basis of the trifid state of the forewing medial With more than 40,000 described species and veins and the horizontally oriented thoracic tym- possibly as many undescribed, the Noctuoidea, pana without counter‐tympanal hoods (Miller currently arranged into six families, represent the 1991). The remaining noctuoids exhibit a quadri- most species‐rich lepidopteran superfamily, with fid condition in the forewing and obliquely ori- more than 25% of described Lepidoptera. They ented tympana with counter‐tympanal hoods. account for the largest family cohort of spe- Although the noctuoids had undergone numer- cies (> 1000), including the bollworms ous rearrangements, Arctiidae and Lymantriidae (), the most economically important remained intact as separate families while the so‐ insect pests worldwide. Noctuoids are character- called deltoid subfamilies (underwings and their ized by larval crochets arranged in uniordinal relatives) were retained within the Noctuidae mesoseries and by adult thoracic tympanal proper. These latter groups were differentiated 488 Insect Biodiversity: Science and Society

from so‐called trifine noctuids in part by a quad- 13.6 Needs and Challenges rifine condition in the hindwing analogous to for Advancing Lepidopteran that in the forewing, and it became increasingly Studies clear that they bore more in common with each other than with typical Noctuidae. Following an Developing phylogenetic information is crucial analysis of molecular data that supported earlier to exploring an extensive range of questions. Still findings of Mitchell et al. (2006) and Weller et al. largely unexplored are the roles of climate shifts (1994), Zahiri et al. (2011) faced the alternatives in the evolution of diapause, diet breadth, and of either uniting the lymantriids and arctiids within the Noctuidae to retain its monophyly, or life‐history timing. Broad patterns in the evolu- cleaving the Noctuidae into multiple monophyl- tionary lability of host associations and what etic families. Either alternative, inevitably, would mediates diet breadth have not been explored in render the Arctiinae and Lymantriinae as sub- detail. Likewise, major questions remain regard- families. Rather than create a vastly expanded ing timing of evolutionary events involving the Noctuidae, the decision, therefore, was made to origins of echolocation, the coevolutionary circumscribe a monophyletic Erebidae to include chemical arms race, the mechanics of mimicry, deltoid subfamilies as well as Arctiinae and and the relationships between major climatic Lymantriinae (Zahiri et al. 2011), and elevate the shifts and the appearance and disappearance of noctuid subfamilies and Euteliinae to major moth and butterfly groups. These endeav- family rank. This arrangement restricts the still‐ ors require insight from a wide variety of fields, enormous Noctuidae to a core of subfamilies including those external to entomology. Regier bearing trifine venation, although exceptions et al. (2013) mention three trends: increasing ultimately might destabilize this classification. body size, the transition from endophytophagy Recent analyses of relationships among the to concealed external feeding and thence to quadrifid noctuoid families have varied (cf. exposed external feeding, and sound detection. Zahiri et al. 2011, 2012, 2013a, 2013b; Yang et al. A fourth is a proliferation in the number of ori- 2015). In their coverage of the Nolidae, Zahiri gins of diurnality and aposematism (visual and et al. (2013b) recovered support for the arrange- acoustic) in association with the allelochemicals ment [Oenosandridae + [Notodontidae + [Eute synthesized de novo or coopted from chemically liidae + [Erebidae + [Noctuidae + Nolidae]]]]]. defended host plants. The ways in which Because of the widespread familiarity of noctu- Müllerian mimicry rings are amplified over ids sensu lato, these rearrangements have been macroevolutionary time have not been explored accepted slowly. In terms of species richness, adequately, nor have higher‐level phylogenetic the result is that the Noctuidae have been trends of co‐mimetics. But the repeated origins reduced by more than 50%, from roughly 25,000 of similar patterns among moth and butterfly to 12,000 species, the remainder combined with groups with widely disparate origins is notewor- Arctiinae and Lymantriinae to form the Erebidae thy, including the ­convergence toward butterfly of nearly 25,000 species or distributed within patterns within groups both ancestrally derived the elevated Euteliidae and Nolidae. Significant (e.g., Zygaenidae: Chalcosiinae) and more strides have been made in resolving relation- recently derived (e.g., Epicopeiidae) with respect ships within Erebidae (Zahiri et al. 2012) and to the butterflies themselves. Nolidae (Zahiri et al. 2013b). The tribal and sub- At a time when advances in bioinformatics, familial classification of the trifines, the data mining, and especially genomic research Noctuidae sensu stricto, is a highly unstable coincide with unparalleled loss of habitat, a press- taxonomic morass, but one likely to congeal in ing need exists for deep phylogenetic research, the upcoming years. basic alpha taxonomy, and faunal inventory alike. 13 Diversity and Significance of Lepidoptera 489

Genomic data will be crucial for elucidating rela- and that many groups of organisms will one day tionships among lepidopteran groups, but will be known only from preserved specimens and need to be coupled with careful comparative work tissues. We do not suggest that systematists will to better understand the origins of insect‐life his- assume the roles of biological morticians. Short tories and how they reflect the history of the of proposing major infrastructural overhauls to planet. Such efforts also will be crucial for stabi- the way resources are allocated to biological lizing nomenclature across continents where research, we might at least redouble our explor- closely related species have been isolated in atory and expeditionary efforts in the more monobasic genera (Mikkola et al. 1991). And so, diverse and threatened regions, adopt tech- although it will be critical to accelerate the pace of niques for collecting and indefinitely preserving evolutionary research, systematics requires genomic‐grade tissues of as many taxa as possi- greater use of and more rigorous analyses of even ble, and mount efforts to identify diverse and rudimentary molecular genetic data, such as under‐sampled groups and generate baseline DNA barcodes, not simply for purposes of raw faunistic data as efficiently as possible. description but for formal diagnostic purposes. For Lepidoptera, and insects in general, the age of discovery is far from over. Major groups ­Acknowledgments of small and large moths alike might have fewer than 50% of their species described. Even with John Brown and Gary Miller reviewed drafts of the integration of molecular data for purposes this manuscript and made numerous construc- of discovery and description (Goldstein and tive suggestions. Don Davis, Maria Heikkila, DeSalle 2011), the documentation of life‐history and John Brown made especially helpful sugges- information required to answer evolutionary tions on treating microlepidopteran and ecological questions is both daunting and classification. even more time sensitive than the collection of specimen material. Unfortunately, dwindling resources might not be adequate to maintain ­References existing natural history collections that make phylogenetic and evolutionary research Barber, J. R. and W. E. Conner. 2007. Acoustic possible. mimicry in a predator‐prey interaction. As the pace of scholarship enables empirical Proceedings of the National Academy of and analytical shortcuts, it will be important to Sciences USA 104: 9331–9334. ensure that the novelty of genomic data does Barber J. R. and A. Y. Kawahara. 2013. not fuel the confusion of phylogenetic systemat- Hawkmoths produce anti‐bat ultrasound. ics with simple nomenclature (Costello et al. Biology Letters 9: 20130161. 2013; cf. de Carvalho et al. 2013). Although a Barber, J. R., B. C. Leavell, A. L. Keener, J. W. growing number of tools have been developed Breinholt, B. A. Chadwell, C. J. W. McClure, G. and are being brought to bear on entomological M. Hill and A. Y. Kawahara. 2015. Moth tails research generally and systematic and taxo- divert bat attack: Evolution of acoustic nomic work in particular, systematic entomol- deflection. Proceedings of the National ogy is struggling with an increasingly rarefied Academy of Sciences USA 112: 2812–2816. professional climate and dwindling funding Bernays, E. A. and D. H. Janzen. 1988. Saturniid resources at a time when biological diversity is and sphingid caterpillars: two ways to eat threatened more directly than ever before. If we leaves. Ecology 69: 1153–1160. are to be realistic, we must acknowledge that the Boettner G. H., J. S. Elkinton and C. J. Boettner. current extinction crisis is not likely to abate, 2000. Effects of a biological control 490 Insect Biodiversity: Science and Society

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