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The Radiation of Satyrini Butterflies (Nymphalidae: Satyrinae): A

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The Radiation of Satyrini Butterflies (Nymphalidae: Satyrinae): A Zoological Journal of the Linnean Society, 2011, 161, 64–87. With 8 figures The radiation of Satyrini butterflies (Nymphalidae: Satyrinae): a challenge for phylogenetic methods CARLOS PEÑA1,2*, SÖREN NYLIN1 and NIKLAS WAHLBERG1,3 1Department of Zoology, Stockholm University, 106 91 Stockholm, Sweden 2Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Av. Arenales 1256, Apartado 14-0434, Lima-14, Peru 3Laboratory of Genetics, Department of Biology, University of Turku, 20014 Turku, Finland Received 24 February 2009; accepted for publication 1 September 2009 We have inferred the most comprehensive phylogenetic hypothesis to date of butterflies in the tribe Satyrini. In order to obtain a hypothesis of relationships, we used maximum parsimony and model-based methods with 4435 bp of DNA sequences from mitochondrial and nuclear genes for 179 taxa (130 genera and eight out-groups). We estimated dates of origin and diversification for major clades, and performed a biogeographic analysis using a dispersal–vicariance framework, in order to infer a scenario of the biogeographical history of the group. We found long-branch taxa that affected the accuracy of all three methods. Moreover, different methods produced incongruent phylogenies. We found that Satyrini appeared around 42 Mya in either the Neotropical or the Eastern Palaearctic, Oriental, and/or Indo-Australian regions, and underwent a quick radiation between 32 and 24 Mya, during which time most of its component subtribes originated. Several factors might have been important for the diversification of Satyrini: the ability to feed on grasses; early habitat shift into open, non-forest habitats; and geographic bridges, which permitted dispersal over marine barriers, enabling the geographic expansions of ancestors to new environ- ments that provided opportunities for geographic differentiation, and diversification. ‘To a man with a hammer, everything looks like a nail’. Mark Twain © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161, 64–87. doi: 10.1111/j.1096-3642.2009.00627.x ADDITIONAL KEYWORDS: Bayesian – biogeography – diversity – grasses – habitat shift – host plants – likelihood – parsimony. INTRODUCTION Wahlberg & Freitas, 2007; Peña & Wahlberg, 2008), Papilionidae (Braby, Trueman & Eastwood, 2005; The evolutionary history of butterflies (Hesperioidea Nazari et al., 2007), and Pieridae (Braby, Vila & and Papilionoidea) has been largely a mystery. The Pierce, 2006; Wheat et al., 2007). Butterflies in the lack of robust phylogenetic hypotheses and a tempo- subfamily Satyrinae include some 2500 species of ral framework (Vane-Wright, 2004) has inhibited the worldwide distribution (Ackery, de Jong & Vane- study of aspects of the evolution of butterflies, such as Wright, 1999). Despite the high number of species biogeographical events and evolution of adaptive this group has been largely neglected: in particular, traits. It is only recently that studies using molecular there have been very few phylogenetic studies. The methods have provided time estimates for the origin only phylogenetic hypothesis available for the group and diversification of butterflies in the Nymphalidae as a whole reveals that Satyrinae as traditionally (Wahlberg, 2006; Kodandaramaiah & Wahlberg, 2007; construed is a polyphyletic entity in need of taxo- nomic revision (Peña et al., 2006). Peña et al. (2006) *Corresponding author. E-mail: [email protected] and Peña & Wahlberg (2008) show that the bulk of 64 © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161, 64–87 THE RADIATION OF SATYRINI BUTTERFLIES 65 Satyrinae species are included in one clade, the tribe Holarctic, Palaearctic (Dennis & Eales, 1997), and Satyrini, that encompasses approximately 2200 Oriental regions (Kodandaramaiah & Wahlberg, species. 2009), and in tropical habitats in Indo-Australia The species of Satyrini, now distributed worldwide, (Braby, 1993; Kodandaramaiah et al., 2009). Members began to diversify about 36 Mya, in the Late Eocene, of the subtribe Parargina occur in woodland, wooded almost simultaneously with the rise and spread of savannahs, and forests of Europe, North Africa, and grasses (Peña & Wahlberg, 2008). In a previous study temperate Asia (van Swaay, Warren & Loïs, 2006; (Peña & Wahlberg, 2008), we proposed that ancestral Konvicka et al., 2008). Maniolina is found in moist Satyrinae inhabited the ubiquitous dicotyledonous- meadows and forest edges (Billeter, Sedivy & Dieköt- dominated forests of the Paleocene and Eocene, ter, 2003) in the Palaeartics and Asia. The only genus feeding on early monocots and basal Poales. We in Melanargiina, Melanargia, has a Palaearctic dis- speculated that the mostly grass-feeding tribe tribution, inhabiting grasslands from Western Europe Satyrini was able to diversify, and spread throughout to Asia and North Africa (Vandewoestijne et al., 2004). the world, after shifting habitats from dicotyledonous The subtribe Mycalesina occurs in the understory of forests to the grasslands and savannahs (Peña & marginal forests and secondary vegetation in Africa Wahlberg, 2008) that have replaced vast areas of and Indo-Australia, and some taxa extend into tem- forest since the Oligocene (33–26 Mya) (Willis & perate Asia. Erebiina can be found in the Holarctic McElwain, 2002). Peña & Wahlberg (2008) did not region, mostly in alpine or arctic areas (Albre et al., draw major conclusions on the evolution of the lin- 2008). Satyrina is found in grassland habitats (van eages in the Satyrini because of limited taxon sam- Swaay et al., 2006) in Europe, Asia, and North pling: we only included 33 Satyrini species out of America, and some species are found in North Africa. 2200. In order to investigate the diversification of this Members of the Lethina (sensu Peña et al., 2006) are diverse and interesting group of butterflies, a denser found in woodland areas (Ide, 2002) and grasslands of taxon sampling is necessary to discover which factors Europe, Africa, Asia, and Indonesia, and some taxa are important in the spectacular radiation of Satyrini. are found in North America. The Ypthimina occurs in open area habitats such savannahs (Sourakov & Emmel, 1997) in Asia, New Caledonia, Africa, and DISTRIBUTION PATTERNS Indonesia. Satyrini butterflies are distributed worldwide, with the highest diversity found in tropical regions. The 13 Satyrini subtribes include 209 genera, with some HISTORICAL BIOGEOGRAPHY subtribes being almost entirely restricted to single The global distribution of Satyrini, combined with the biogeographical regions. These butterflies inhabit more restricted nature of most of the subtribes, sug- temperate and tropical habitats around the world: gests that a biogeographic study of the group could be occuring in most habitats from lowland savannahs informative for understanding the evolution and and rainforests to high-elevation cloud forests and radiation of other butterfly and insect groups. grasslands (páramos and puna; Viloria, 2003), alpine Miller (1968), in his important taxonomic revision and arctic areas in the Holarctic (Albre, Gers & Legal, of the entire Satyrinae, proposed an evolutionary tree 2008), tropical lowland habitats in the Oriental and for the higher taxa in the Satyrinae, and detailed a Australian regions (Braby, 1994), and grasslands and biogeographic scenario for the evolution of the group. woodlands in Africa (Fitzherbert et al., 2006). In a phylogenetic study of Pronophilina and the New The Pronophilina inhabits Andean cloud forest Zealand endemic Argyrophenga antipodum Double- environments from Venezuela to Bolivia, from day, 1845, Viloria (2003, 2007b) stated that his data 1400 m a.s.l. up to the border of the páramos at set supported a close relationship between southern 3200–3400 m a.s.l. (Pyrcz & Wojtusiak, 2002). The temperate pronophilines and Argyrophenga. Viloria subtribe Euptychiina was thought to be entirely (2003, 2007b) proposed that subtribes in the Satyrini restricted to the Americas (Miller, 1968; Murray & originated in Gondwana, and that after the break-up Prowell, 2005); however, there is mounting evidence of that land mass (c. 60 Mya) some members of Eup- that the Oriental Palaeonympha opalina Butler, 1871 tychiina and Hypocystina remained in South belongs to this subtribe, as suggested by morphologi- America. Later on, the Pronophilina diverged from cal characters (Miller, 1968) and molecular data the Hypocystina and colonized Mesoamerica and the (Peña et al., 2006). The euptychiines are distributed Caribbean Islands by 10–3 Mya. Unfortunately, in lowland and cloud forest habitats from central USA Viloria (2003, 2007b) based his biogeographical con- to Argentina (Murray & Prowell, 2005). The clusions on erroneous interpretations of his phyloge- Coenonymphina (formerly Hypocystina) includes rep- netic trees. In the caption of his figure 1, Viloria resentatives that inhabit oligotrophic mires in the (2003: 248) writes: ‘New Zealand Argyrophenga © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161, 64–87 66 C. PEÑA ET AL. antipodum is included as the out-group, and its Satyrini genera (out of 209) from all subtribes in the closest species is the Chilean endemic Argyrophorus Satyrini, following the classifications of Miller (1968) argenteus’ (his tree had A. argenteus as the top-most and Peña et al. (2006). As there is no phylogenetic species of a monophyletic neotropical clade, simply hypothesis available for all genera in Satyrini, we
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