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A Classification of Danaus Butterflies (Lepidoptera: Nymphalidae)

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A Classification of Danaus Butterflies (Lepidoptera: Nymphalidae) Blackwell Science, LtdOxford, UKZOJZoological Journal of the Linnean Society0024-4082The Lin- nean Society of London, 2005? 2005 1442 191212 Original Article CLASSIFICATION OF DANAUSD. A. S. SMITH ET AL. Zoological Journal of the Linnean Society, 2005, 144, 191–212. With 3 figures A classification of Danaus butterflies (Lepidoptera: Nymphalidae) based upon data from morphology and DNA DAVID A. S. SMITH FLS1*, GUGS LUSHAI FLS2 and JOHN A. ALLEN FLS2 1Natural History Museum, Eton College, Windsor SL4 6EW, UK 2Ecology & Biodiversity Division, School of Biological Sciences, University of Southampton SO16 7PX, UK Received September 2003; accepted for publication March 2005 Classification of the cosmopolitan butterfly genus Danaus (Nymphalidae: Danainae) is revised at subgeneric, specific and subspecific levels, combining for the first time mitochondrial and nuclear DNA sequence information with mor- phological data. Tree topologies based on the nuclear genome (allozymes, pheromone components, the morphology of all life history stages and nuclear DNA sequences), on the one hand, and mitochondrial DNA, on the other, are incon- gruent and challenge the current taxonomy of the genus. Although earlier classifications, based on adult morphology alone, are, in general, well supported by an analysis of total evidence, the mitochondrial phylogeny shows that the species D. chrysippus and its subgenus Anosia are deeply paraphyletic. Subspecies dorippus of D. chrysippus is the basal clade of the genus and is reinstated as the species D. dorippus. The former species D. plexaure is demoted to a subspecies of D. eresimus. The specific status of D. erippus, as distinct from D. plexippus, is tentatively supported. On the strength of the new data, division of the monophyletic genus Danaus s.l. into three subgenera Danaus s.s., Salatura and Anosia is unsustainable and is abandoned. Of the 15 terminal clades (taxa) of Danaus s.l. included in the study, 11 are species that broadly conform to the biological species concept. (The West Indian species D. cleophile, missing from our analysis, is the twelfth species). The remaining terminal clades are subspecies of D. chrysippus comb. nov. and D. dorippus stat. rev. Two sympatric Neotropical species, D. eresimus and D. gilippus, are mor- phologically distinct and sexually isolated but have nearly identical mitochondrial genomes. In contrast, two partially sympatric Palaeotropical species, D. chrysippus and D. dorippus, are cryptic species that share structural morphology and hybridize but have highly differentiated mitochondrial genomes. D. dorippus is polymorphic for two anciently diverged haplotypes and its history has possibly involved recombinational speciation and/or hybridism. © 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 144, 191-212. ADDITIONAL KEYWORDS: Anosia – cryptic species – hybridism – male killing – paraphyly – recombinational speciation – Salatura – Spiroplasma – subspecies – sympatric speciation. INTRODUCTION D. chrysippus (L.) was depicted in a fresco on an Egyp- tian tomb some 3500 years ago (Larsen, 1977, 1984) Danaus species are among the most apparent and and became the first recorded butterfly in history. Of abundant of all butterflies. A predominantly tropical 11 Danaus species recognized today (Ackery & Vane- group, all the species are medium to large in size and, Wright, 1984; hereinafter A & V-W), Linnaeus (1758) with the exception of ismare (Cramer) and some sub- was able to name among his Danai Festivi only species of melanippus (Cramer) and affinis (Fabricius), plexippus (L.) and chrysippus (L.) (as species of sport gaudy colour schemes comprising an orange, yel- Papilio). These two, together with genutia (Cramer) low or brown ground colour with bold black and white (which Linnaeus confounded with plexippus), eresimus markings. The genus has enjoyed icon status ever since (Cramer) and gilippus (Cramer), frequently abound in the vicinity of human settlements. *Corresponding author. 4 Buttercup Meadow, Clyro, Hereford The confident lifestyle that combines advertise- HR3 5JZ, UK. E-mail: [email protected] ment, relaxed flight and pungent odour serves to deter © 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 144, 191–212 191 192 D. A. S. SMITH ET AL. potential predators from launching damaging attacks. Subtribe Genus Subgenera Species Defences of last resort are the exceptionally tough Tirumala exoskeleton and acrid flavour that birds encounter when attempting to remove the wings as a prelude to (Danaus) devouring the body. The repellent and toxic qualities cleophile of Danaus butterflies derive in part from cardiac gly- plexippus cosides or cardenolides (CGs) that are sequestered by Danaus erippus Danaina the larvae of some species from their predominantly (Salatura) ismare milkweed (Asclepiadaceae) foodplants and subse- genutia quently stored in all life history stages (Brower, affinis melanippus Brower & Corvino, 1967; Rothschild et al., 1975). CGs (Anosia) eresimus are not only enduringly distasteful, implanting an plexaure indelible memory in the predator’s brain, but are also gilippus powerful emetics (Brower, 1984) and dangerous heart chrysippus stimulants (Parsons, 1965). CG defence may be supplemented or supplanted by Figure 1. Cladistic reconstruction of the genus Danaus, bitter-tasting pyrrolizidine alkaloids (PAs) that are after Ackery & Vane-Wright (1984). sequestered by adults of both sexes (but especially avidly by males) from plant genera such as Parsonsia Amaurina and Danaina. The only exceptions were (Apocynaceae), Tournefortia and Heliotropium (Borag- some 15 species of Amauris Hübner and four Ideopsis inaceae), Crotalaria (Fabaceae), Erechtites, Gynura Horsfield (Talbot, 1940a, b, 1943). However, A & V-W, and Senecio (Asteraceae). PAs are precursors for in consensus with some Japanese workers, promoted intrinsic components of the male pheromone or ‘love- the Danaus subgenera Parantica Moore and Tirumala dust’ that is transferred by abdominal hair-pencils to Moore to generic rank and transferred to them, the antennae of the female during courtship (Boppré, respectively, 38 and nine former Danaus species. Four 1984). However, nonmetabolized PAs are also stored in Danaus (Radena Moore) were moved to Ideopsis; thus adult tissues, are passed to females in spermatophores enlarging the latter to eight species. Danaus s.l. and comprise up to 5% of male body mass in remained with just 11 species divided among three D. chrysippus (J. Edgar, pers. comm.); as potent liver noncoordinate subgenera, Danaus s.s. (three species), toxins in vertebrates (Bull, Culvenor & Dick, 1968), Salatura Moore (four species) and Anosia Hübner PAs undoubtedly fulfil a defensive as well as a sexual (four species). role (Edgar et al., 1976, 1979). A & V-W explicitly sought to provide a sound generic When Bates (1862) in South America, followed by classification of the subfamily Danainae (now tribe Wallace (1865) in the Orient, Trimen (1869) in Africa Danaini); for the most part they accepted previous and Walsh & Riley (1869) in North America, estab- decisions by Talbot (1940a, b, 1943), Corbet (1943) and lished the notion of Batesian mimicry (as it is now others on what, in their words, ‘constitutes a danaine known), Danaus butterflies were immediately recog- species’. They did, however, provide a cladistic analy- nized as models with many mimics. After Müller sis of relationships among Danaus species (Fig. 1) and (1878) had extended the mimicry theme to include the commented on relationships that were indistinguish- convergent evolution of warning coloration among dis- able in their analysis, for example between D. affinis tasteful species (now known as Müllerian mimicry), (Fabricius) and D. philene (Stoll). Here, our principal Moore (1883) demonstrated in extensive comparative aim is to reappraise the classification of Danaus s.l. at tables that the latter concept (to which he made no subgeneric, specific and subspecific levels, bringing explicit reference) was highly relevant to danaine together for the first time the morphological charac- butterflies. ters used by A & V-W, data on allozymes, early stages Various names for Danaus butterflies in vernacular and colour genes published subsequently to A & V-W, English include monarch, queen, wanderer and tiger. and our own DNA sequence data from both mitochon- The generic name Danaus Kluk, 1802 (family Nymph- drial and nuclear genomes. alidae, subfamily Danainae, tribe Danaini, subtribe Danaina) (Harvey, 1991; see also Wahlberg, Weingart- ner & Nylin, 2003b) was unstable until Hemming MATERIAL AND METHODS (1933) established it. Prior to the latest generic level MORPHOLOGICAL DATABASE revision of the milkweed butterflies (tribe Danaini) by A & V-W (as subfamily Danainae), in most previous The morphological data-base (Appendix 1A, B) is presentations the Danaus umbrella had embraced the assembled from published sources as follows: char- majority of c. 81 species now belonging to subtribes acters from adult butterflies, including dihydropyr- © 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 144, 191–212 CLASSIFICATION OF DANAUS 193 Table 1. Provenance, voucher numbers [OUMNH] of individual butterflies used for analysis of DNA sequences and sample sizes for each sequence1 included in this paper Sample Sizes Provenance and Species & subspecies voucher numbers […]1 12S + COI7 18S EF1-a Amauris niavius niavius Tanzania [640] – – 1 A. dannfelti dannfelti
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