463 13 Diversity and Significance of Lepidoptera: A Phylogenetic Perspective Paul Z. Goldstein Systematic Entomology Laboratory, Plant Science Institute, Agriculture Research Service, US Department of Agriculture, c/o Smithsonian Institution, Washington, DC, USA The Lepidoptera – moths, butterflies, and skip- aggressive mimicry. Ecologically, butterflies and pers – represent one of the three most species‐ moths constitute a primary food source for diur- rich insect orders and the largest evolutionary nal and nocturnal vertebrate insectivores, serve radiation of herbivorous animals (Scoble 1992, as hosts for innumerable specialist insect parasi- Wahlberg et al. 2013). The Jurassic 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 plants, 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 biodiversity, 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 Cretaceous 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 parasitoids. From the societal standpoint, lepidopterans Their morphological, physiological, and behav- provide obvious resources, silk 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 leaf miners, leaf rollers, and stem bor- Because they respond quickly to environmental ers, stand out among the holometabolous insects change, including climatic and atmospheric as conspicuous participants in the evolutionary shifts and landscape alteration, Lepidoptera dynamics of defensive behaviors, crypsis, 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 taxonomy and diversity: and aposematism, 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 moth 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 pheromone 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 (Nymphalidae; Gilbert 1984, Brower (Zahiri et al. 2014). To the extent that fresh speci- 1996), dioptine prominent moths (Notodontidae; mens can be determined reliably in the field, Miller 1996, 2009), and other winged insects, genome‐grade tissues may be amassed more effi- many of which share passion flowers ciently than for many invertebrate groups, and (Passifloraceae) as larval hosts. Yucca and yucca phylogenomic progress is likely to be rapid in moths (Prodoxidae) 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 areas and aiding the assessment of conservation insects. Genes responsible for butterfly 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