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The Phylogenetic Relationships of Chalcosiinae (Lepidoptera, Zygaenoidea, Zygaenidae)

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The Phylogenetic Relationships of Chalcosiinae (Lepidoptera, Zygaenoidea, Zygaenidae) Blackwell Science, LtdOxford, UKZOJZoological Journal of the Linnean Society0024-4082The Lin- nean Society of London, 2005? 2005 1432 161341 Original Article PHYLOGENY OF CHALCOSIINAE S.-H. YEN ET AL. Zoological Journal of the Linnean Society, 2005, 143, 161–341. With 71 figures The phylogenetic relationships of Chalcosiinae (Lepidoptera, Zygaenoidea, Zygaenidae) SHEN-HORN YEN1*, GADEN S. ROBINSON2 and DONALD L. J. QUICKE1,2 1Division of Biological Sciences and Centre for Population Biology, Imperial College London, Silwood Park Campus, Ascot, Berkshire, SL5 7PY, UK 2Department of Entomology, The Natural History Museum, London SW7 5BD, UK Received April 2003; accepted for publication June 2004 The chalcosiine zygaenid moths constitute one of the most striking groups within the lower-ditrysian Lepidoptera, with highly diverse mimetic patterns, chemical defence systems, scent organs, copulatory mechanisms, hostplant uti- lization and diapause biology, plus a very disjunctive biogeographical pattern. In this paper we focus on the genus- level phylogenetics of this subfamily. A cladistic study was performed using 414 morphological and biochemical char- acters obtained from 411 species belonging to 186 species-groups of 73 genera plus 21 outgroups. Phylogenetic anal- ysis using maximum parsimony leads to the following conclusions: (1) neither the current concept of Zygaenidae nor that of Chalcosiinae is monophyletic; (2) the previously proposed sister-group relationship of Zygaeninae + Chal- cosiinae is rejected in favour of the relationship (Zygaeninae + ((Callizygaeninae + Cleoda) + (Heteropan + Chalcosi- inae))); (3) except for the monobasic Aglaopini, none of the tribes sensu Alberti (1954) is monophyletic; (4) chalcosiine synapomorphies include structures of the chemical defence system, scent organs of adults and of the apodemal system of the male genitalia. A paired metathoracic androconial organ and a series of abdominal tergal corematal organs have been discovered, both being new to Lepidoptera. Due to highly homoplastic patterns in copulatory structures and wings that demonstrate significant sexual dimorphism, polymorphism and mimicry, 17 of the 69 ‘true’ chalcosiine genera (c. 25%) are shown to be either paraphyletic or polyphyletic. The present classification is therefore very mis- leading. Reductions of various parts of the male genitalia in some groups are accompanied by morphological and func- tional replacement involving the 8th abdominal segment. A prominent but convergent lock and key mechanism is revealed. © 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 143, 161–341. ADDITIONAL KEYWORDS: chaetosoma – chemical defence – constraint analysis – cyanogenesis – genitalic reduction – mimicry. INTRODUCTION from stable, including from seven (Scoble, 1992) to 13 families (Epstein et al., 1999), and its monophyly is HISTORICAL REVIEW OF HIGHER CLASSIFICATION still highly debatable (Fig. 1). OF ZYGAENOIDEA Dyar (1894) brought Limacodidae (as Eucleidae), Like many other superfamilies within the ditrysian Megalopygidae, Zygaenidae and Procridinae (as Lepidoptera, the Zygaenoidea are not characterized by Pyromorphidae) into an assemblage called the ‘Anth- clearly defined autapomorphies (Epstein et al., 1999). rocerina’ based on larval chaetotaxy, which was The taxon appears at first glance to have become a subsequently combined with ‘Cossina’ within the wastebasket, including a number of family groups superfamily ‘Tineides’ (Dyar, 1896). Chapman (1893, that may individually be well defined, but do little 1894) lumped the Zygaenidae with Limacodidae (as more than share a number, albeit numerous, of plesi- Cochliopodidae) and Micropterigidae into the pupal omorphic characters. Its composition has been very far group ‘Incompletae’, although these views were not accepted by most authors at that time (Dyar & Mor- ton, 1895; Packard, 1895, Hinton, 1955). *Corresponding author. Current address: Department of In 1895, Packard suggested a close relationship Biological Sciences, National Sun Yat-Sen University, 70 Lien-hai Rd, Kaohsiung 804, Taiwan. E-mail: between Limacodidae and Megalopygidae, but he [email protected] placed them under Tineina, and thus apart from the © 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 143, 161–341 161 162 S.-H. YEN ET AL. Zygaeninae Dalceridae Phaudinae Phaudinae Epipyropidae Megalopygidae Charideinae Cyclotornidae Somabrachyidae Callizygaenini Megalopygidae Anomoeotidae Procridini Limacodidae Himantopteridae Himantopterinae Chrysopolomidae Epipyropidae Anomoeotinae Procridinae Cyclotornidae A Chalcosiinae Zygaeninae Aididae Charideinae Limacodidae Phaudinae Dalceridae Himantopterinae Lacturidae Anomoeotinae Heterogynidae Megalopygidae D Chalcosiinae Callizygaeninae Limacodidae Somabrachyidae Procridinae Chrysopolomidae Cyclotornidae Zygaeninae Epipyropidae Epipyropidae G Chalcosiinae Cyclotornidae Megalopyginae Megalopygidae Heterogynidae Trosiinae Somabrachyidae Lactura-group Aididae Anomoeotidae Phaudinae Dalceridae Himantopteridae Anomoeotinae Pant/Croth Epipyropidae Himantopterinae Chrysopolominae Cyclotornidae Charideinae Limacodinae Aididae Procridinae Zygaenidae Limacodidae E Dalceridae Zygaeninae Bombycina Lacturidae B Chalcosiinae Tortricoidea Heterogynidae Castnioidea Phaudinae Other Cossoids Callizygaeninae Cyclotornidae Procridinae Epipyropidae Zygaeninae Charideinae Dalceridae Chalcosiinae (Thyrididae) Chrysopolomidae H Megalopygidae Epipyropidae Limacodidae Aididae Cyclotornidae Tineina Limacodidae Dalceridae Sesioidea Dalceridae Limacodidae Somabrachyidae Epipyropidae Chrysopolomidae Megalopygidae Himantopteridae Megalopygidae Heterogynidae Lacturidae Anomoeotidae Lacturidae Phaudinae Himantopteridae Himantopteridae Procridinae Heterogynidae Anomoeotinae Callizygaeninae Procridinae Phaudinae Zygaenidae Zygaeninae Procridinae I Chalcosiinae C Chalcosiinae Zygaeninae F Chalcosiinae Figure 1. Schematic classifications and phylogenetic concepts of Zygaenoidea and Zygaenidae proposed by differ- ent authors. In each of the hypotheses, members of Zygaenidae are in bold and non-zygaenoid groups are in italic. A, Alberti (1954). B, Minet (1986, 1991, 1994). C, Common (1970) and Nielsen & Common (1991). D, Scoble (1992). E, Epstein (1996). F, Heppner (1998). G, Fänger et al. (1999). H, Epstein et al. (1999). I, Holloway et al. (2001). Zygaenidae. The term ‘Zygaenoidea’ was first intro- 1990; Kuznetzov & Stekolnikov, 1981; Minet, 1986; duced by Fracker (1915), who included within it Scoble, 1992). Chalcosiinae (as Chalcodidae [sic]), Procridinae (as Except for Zygaenidae, Brock (1971) placed most Pyromorphidae), Epipyropidae, Dalceridae, Megalopy- families previously assigned to Zygaenoidea in the gidae, and Limacodidae. This classification has been Cossoidea, based primarily on characters of the adult expanded by modern workers to include all of the cur- thorax and forewings. He also transferred Epipyropi- rent family groups of Zygaenoidea (Common, 1975, dae and Heterogynidae to the Tineoidea. Heppner © 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 143, 161–341 PHYLOGENY OF CHALCOSIINAE 163 (1984, 1992, 1998) retained Megalopygidae, Som- Tarmann & Tremewan (1999) and Epstein et al. abrachyidae, and Heterogynidae in Zygaenoidea, but (1999), the current concept of zygaenids is not sup- placed Epipyropidae, Cyclotornidae, and the remain- ported by general morphological features but rather der of the limacodid group (see below) in the Cos- by their ability to synthesize two cyanogenic com- soidea. Brock’s Cossoidea, except for the position of pounds from the amino acids valine and isoleucine Epipyropidae and Heterogynidae, has been followed (Witthohn & Naumann, 1984a, b, 1987a, b; Epstein by Fletcher & Nye (1982). Brock did not provide jus- et al., 1999; Naumann et al., 1999). tification for this arrangement. This classification has The chemical defence ecology of Zygaenidae was been criticized, however, both for the weakness of the first reported by Jones et al. (1962) who demonstrated adult characters involved and because of the strength that HCN is released from crushed tissues of all of the immature stage characters as evidence for the instars of Zygaena filipendulae, and that the highest monophyly of Zygaenoidea in its earlier sense (Com- concentrations of HCN precursors are found in the mon, 1975; Kuznetzov & Stekolnikov, 1981). eggs. Subsequently, various studies on the biochemical Minet (1986, following Common, 1975), proposed mechanisms, interactions amongst hostplants, moths two potential autapomorphies of Zygaenoidea: the and their parasitoids, and the relevant morphological retractile head of the larva (at least in the later structures of several representative genera of Zyga- instars); and the position of the second abdominal spi- enidae were conducted by a number of research teams. racle of the pupa, which is covered by the wings. The The chemical source of HCN in Burnet moths latter character has been verified for Epipyropidae, remained unknown until Davis & Nahrstedt (1979) Megalopygidae (including Somabrachyidae), Limaco- demonstrated that it is derived from two cyanogluco- didae, Heterogynidae, Zygaenidae (Epstein et al., sides, linamarin and lotaustralin. Linamarin and 1999), Cyclotornidae, Himantopteridae and Zyga- lotaustralin have long been known to occur in a num- enidae (Fänger, Yen & Naumann, 1999). Although it ber of plant families, e.g. Fabaceae, widely
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