Molecular Phylogeny and Generic-Level Taxonomy of the Widespread Palaeotropical `Heteropsis Clade' (Nymphalidae: Satyrinae
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Systematic Entomology (2016), 41, 717–731 DOI: 10.1111/syen.12183 Molecular phylogeny and generic-level taxonomy of the widespread palaeotropical ‘Heteropsis clade’ (Nymphalidae: Satyrinae: Mycalesina) KWAKU ADUSE-POKU1,2, DAVID C. LEES1,3, OSKAR BRATTSTRÖM1, ULLASA KODANDARAMAIAH4, STEVE C. COLLINS5, NIKLAS WAHLBERG6,7 andPAUL M. BRAKEFIELD1 1Radiating Butterfly Group, Department of Zoology, University of Cambridge, Cambridge, U.K., 2Department of Biology, City College of New York, City University of New York, New York, NY, U.S.A., 3Department of Life Sciences, Natural History Museum, London, U.K., 4Vanasiri Evolutionary Ecology Group, Indian Institute of Science Education and Research, Thiruvananthapuram, India, 5African Butterfly Research Institute (ABRI), Nairobi, Kenya, 6Department of Biology, University of Turku, Turku, Finland and 7Department of Biology, Lund University, Lund, Sweden Abstract. The mycalesine butterfly genus Heteropsis Westwood, 1850 (Satyrinae: Mycalesina) has recently been conceived to be represented in three major palaeotropical regions (Madagascar, Africa and Asia), but there has been no formal taxonomic treatment covering this entire group. Studies aimed at understanding the evolutionary success of Mycalesina in the Old World tropics have been hampered by the lack of both a robust phylogeny and a stable nomenclature for this satyrine subtribe. Here, we present a well-supported molecular phylogeny based on 10 genes and 133 exemplar taxa, representing almost all known species groups of Heteropsis (s.l.), and including all but four known species in Madagascar. We also combine sequences of the exemplars with a morphological matrix of 428 characters. The widespread ‘Heteropsis clade’ is confirmed as monophyletic, but lineages in different geographic regions also form endemic and well-supported clades with deep divergences among them. Here we establish this group as comprising three genera, Heteropsis (Malagasy region only), Telinga Moore, 1880 (Asia), and Brakefieldia gen.n. (Africa). We recover the genera Telinga and Brakefieldia as sisters with high support. Each genus is taxonomically characterized and a revised synonymic checklist is appended with new combinations and some changes in rank. With a well-resolved topology and updates to the taxonomy of the group, researchers are now in a position to explore the drivers of the spectacular radiation of the group, notably in Madagascar, where the highest phenotypic and species diversity occurs. This published work has been registered in ZooBank, http://zoobank.org/urn:lsid: zoobank.org:pub:AAF9F440-A2D6-4483-BF35-9BC074D9D29B. Introduction systematics (Scotland et al., 2003; Wiens, 2004). Morphological taxonomy has been found to be particularly inadequate in The infusion of molecular data has undoubtedly revolutionized the case of rapid radiations characterized by high diversity of taxonomy. This invaluable toolkit has repeatedly highlighted species and the paucity of species-specific diagnostic traits due shortcomings of traditional morphology-based taxonomy and to relative stasis in the evolution of observable morphological features (Kodandaramaiah et al., 2010b; Van Bocxlaer & Hunt, 2013). The widespread occurrence of such species-rich taxa has Correspondence: Kwaku Aduse-Poku, Radiating Butterfly Group, made taxonomic investigations even more challenging, espe- Department of Zoology, University of Cambridge, Cambridge, U.K and cially because of problems faced in accessing collections housed Department of Biology, City College of New York, City University across several continents. Although butterflies are arguably the of New York, NY 10031, U.S.A. E-mail: [email protected]; kaduse- [email protected] © 2016 The Royal Entomological Society 717 718 K. Aduse-Poku et al. best-studied invertebrates, there are several species-rich groups Region). This trend of using Culapa was, however, followed by whose taxonomy has not been satisfactorily resolved apparently Turlin (1994). Aduse-Poku et al. (2015) showed that the genus due to the above-mentioned issues. One such group is Heterop- Culapa, whose taxonomic scope these authors refined, has no sis Westwood, 1850, which has radiated successfully and rapidly direct relation with the Malagasy region Mycalesina. across the three major biogeographic areas in the Old World Just as the use of Henotesia implies a link between Malagasy tropics. and African Heteropsis (s.l.), Telinga Moore, which was used as Heteropsis was first recognized from Madagascar as the a subgenus in Lees et al. (2003) to include the Malagasy species leaf-mimicking species Heteropsis drepana Westwood. The Heteropsis vola (Ward), assumed a link with Asia. Following the affinities of this taxon were long obscure and intrigued nat- molecular phylogeny of Aduse-Poku et al. (2015), these genus uralists (Wallace, 1876; Miller, 1968). As a result, Heterop- group names can, however, only be treated as endemic within sis has had a confused and complex taxonomic history, from discrete biogeographic regions. The apparently well-supported a monobasic or dibasic genus (Mabille, [1887]; Ackery et al., reciprocal monophylies of the ‘Heteropsis’ lineages on the 1995) to one spanning Madagascar, Africa (Williams, 2014) and, different continents (Aduse-Poku et al., 2015) suggest that more recently, Asia (Kodandaramaiah et al., 2010a; Aduse-Poku the grouping of H. vola and the Oriental taxa in Telinga is et al., 2015). The most recent of these last two treatments incorrect. Likewise the inclusion of the African taxa as part of recognized this ‘hairy-eyed’ (i.e. compound eyes with dense the Malagasy genus Henotesia in some works (Gaede, 1931; intra-ommatidial setae) genus as one of the seven genera that Gabriel, 1932; Van Son, 1955; Usher, 1985; Kielland, 1994; constitute the satyrine subtribe, Mycalesina. This subtribe rep- Ackery et al., 1995; Larsen, 2005; Libert, 2006) is deemed resents a spectacular butterfly radiation of over 300 species in inaccurate. Furthermore, in Madagascar, the internal groupings the Old World tropics (Brakefield, 2010; Kodandaramaiah et al., in Aduse-Poku et al. (2015) for the group are not entirely in line 2010a). Unlike the other mycalesine genera, which are region- with the preceding subgeneric classification proposed by Lees ally highly endemic, Heteropsis spans all major palaeotropical et al. (2003) in the Malagasy Region. In particular, the work regions, with the largest diversification (∼74 species) occurring of Aduse-Poku et al. (2015) shows that Heteropsis fuliginosa in the Malagasy region. The genus currently contains about 110 (Mabille), H. drepana and H. paradoxa (Mabille) were not taxa occurring in both forested and open habitats in the Old placed with their closest relatives. World tropics, and some taxa have wing patterns that stand out Considering groupings in the Asian clade, in addition to from the rest of the subtribe. ‘Mycalesis’ adolphei (Guérin-Ménéville) and ‘Mycalesis’ ocu- The alpha taxonomy of the group in the Malagasy region lus Marshall stated earlier (Lees, 1997; Lees et al., 2003) to be was greatly clarified by Lees (1997), who synonymized 32% part of the genus Heteropsis (as subgenus Telinga,nowren- of the then known species and compensated this taxonomic dered polyphyletic), Kodandaramaiah et al. (2010a) recovered loss with the discovery of about a third (23 undescribed taxa) four additional Asian ‘Mycalesis’ species [M. sangaica (But- of the currently known species on the island. In a follow-up ler), M. mamerta (Stoll), M. malsara (Moore), and M. janardana work, Lees et al. (2003) proposed significant changes to the (Moore)] as nesting within the otherwise Afro-Malagasy ‘Het- higher-level taxonomy for the Malagasy region by organizing eropsis clade’ of their tree (see File S2 with regard to the correct 19 of the then recognized 45 species into five subgenera. The application of the name ‘mamerta’). Aduse-Poku et al. (2015) remaining 26 taxa were, however, considered incertae sedis recovered a further three Mycalesis taxa (M. oculus, M. inopia (with unknown or undefined subgeneric groupings) in this Fruhstorfer, and M. misenus de Nicéville) in the same clade treatment (Lees et al., 2003). Since then, many more (∼25) of (Asian) Heteropsis (s.l.). These two recent studies (Kodan- new taxa of Heteropsis have been discovered in the region, and daramaiah et al., 2010a; Aduse-Poku et al., 2015) sampled about 19 of those are currently being described (e.g. Lees, 2016). half of the (>100) Asian species previously placed in Mycale- Questions such as how the different species groups relate to one sis. In the absence of established morphological synapomor- another phylogenetically and when the important divergences phies, increased molecular sampling of Asian Mycalesis (s.l.) within the group occurred still remain, although Aduse-Poku is clearly needed. This would not only include the (>50) species et al. (2015) provided preliminary answers based on incomplete that Kodandaramaiah et al. (2010a) established as Mydosama, taxon sampling. but also those that Aduse-Poku et al. (2015) further separated The African hairy-eyed mycalesine fauna has traditionally out as ‘true’ Mycalesis or Culapa. Sampling of the African clade been placed in the genus Henotesia Butler (Gaede, 1931; was also not comprehensive enough in Aduse-Poku et al. (2015) Gabriel, 1932; Van Son, 1955; Usher, 1985; Kielland, 1994; to test the species groups of Kielland (1984) in detail, except to Ackery et al., 1995; Larsen, 2005; Libert, 2006). Henotesia