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A Phylogenetic Hypothesis of the Genus Charaxes (Lepidoptera: Nymphalidae) Based on five Gene Regions

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A Phylogenetic Hypothesis of the Genus Charaxes (Lepidoptera: Nymphalidae) Based on five Gene Regions Molecular Phylogenetics and Evolution 53 (2009) 463–478 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Out-of-Africa again: A phylogenetic hypothesis of the genus Charaxes (Lepidoptera: Nymphalidae) based on five gene regions Kwaku Aduse-Poku a,b, Eric Vingerhoedt c, Niklas Wahlberg d,* a Centre for Ecological and Evolutionary Studies, University of Groningen, Kerklaan 30, 9751 NN Haren, The Netherlands b Department of Wildlife and Range Management, Faculty of Renewable Natural Resources, Kwame Nkrumah University of Science & Technology, PMB, Kumasi, Ghana c 35 rue de la Goffe, B-4130 Esneux, Belgium d Laboratory of Genetics, Department of Biology, University of Turku, 20014 Turku, Finland article info abstract Article history: Despite the long popularity of Charaxes among collectors and researchers, their evolutionary history is Received 22 January 2009 largely unknown. The current and accepted species groupings and relationships within the genus are Revised 15 June 2009 based exclusively on adult morphology and life histories. Here, we examine the monophyly and evolu- Accepted 19 June 2009 tionary affinities of the species-groups within the genus Charaxes and explore how they relate to mem- Available online 4 July 2009 bers of their closest genera (Euxanthe, Polyura and Palla) using 4167 bp of sequence data from five (1 mitochondrial and 4 nuclear) gene regions. Within the proposed phylogenetic framework, we estimate Keywords: ages of divergence within the genus and also reconstruct their historical biogeography. We included rep- Molecular systematics resentatives of all known species-groups in Africa and Asia, all known species of Euxanthe and Palla and Africa Historical biogeography two exemplar species of Polyura. We found the genus Charaxes to be a paraphyletic group with regard to Butterflies the genera Polyura and Euxanthe, contrary to the earlier assumption of monophyly. We found that 13 out Timing of divergences of 16 morphologically defined species-groups with more than one species were strongly supported monophyletic clades. Charaxes nichetes is the sister group to all the other Charaxes. Polyura grouped with the Zoolina and Pleione species-groups as a well-supported clade, and Euxanthe grouped with the Lycur- gus species-group. Our results indicated that the common ancestor of Charaxes diverged from the com- mon ancestor of Palla in the mid Eocene (45 million years ago) in (Central) Africa and began diversifying to its extant members 15 million years later. Most of the major diversifications within the genus occurred between the late Oligocene and Miocene when the global climates were putatively undergoing drastic fluctuations. A considerable number of extant species diverged from sister species during the Pliocene. A dispersal–vicariance analysis suggests that many dispersal rather than vicariance events resulted in the distribution of the extant species. The genus Polyura and the Indo-Australian Charaxes are most likely the results of three independent colonizations of Asia by African Charaxes in the Miocene. We synonymize the genera Polyura (syn. nov.) and Euxanthe (syn. nov.) with Charaxes, with the currently circumscribed Charaxes subdivided into five subgenera to reflect its phylogeny. Ó 2009 Elsevier Inc. All rights reserved. 1. Introduction fruits, through dung to carrion, with the last being the most pre- ferred by the males. Charaxes are perhaps the most fascinating The genus Charaxes Ochsenheimer, 1816 (Lepidoptera, Nymp- and admirable group of butterflies in Africa (if not the world). As halidae, Charaxinae) comprises about 250 species distributed Ackery et al. (1999) recount, no group of butterflies in Africa evokes mainly in the African continent with a few (30) occurring in trop- so much passion and emotion as Charaxes. For this reason they have ical Asia and Australia, as well as one species (Charaxes jasius) which long been very popular with collectors. Testament to the extensive extends its range to the Palaearctic. The genus Charaxes is the most fondness for this group of butterflies among collectors is the enor- speciose group of butterflies in Africa apart from Acraea Fabricius mous and readily available ecological information on the group and 1807 (Larsen, 2005). They are generally medium to large sized the existence of a relatively well-known alpha taxonomy. and robust in structure, strong and powerful in flight, ubiquitous Due to the high species richness of Charaxes, taxonomists often in distribution, colorful and showy in appearance and behavior. prefer to summarize and study them under subgroups. Conse- They are also versatile in feeding; their food sources range from quently, species of Charaxes are at the moment placed into 19 puta- tive species-groups in Africa, based almost exclusively on the morphology of the adult (hind)wings (Van Someren, 1963, 1964, * Corresponding author. Fax: +358 2 333 6690. E-mail address: niklas.wahlberg@utu.fi (N. Wahlberg). 1966, 1967, 1969, 1970, 1971, 1972, 1974, 1975; Henning, 1989). 1055-7903/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2009.06.021 464 K. Aduse-Poku et al. / Molecular Phylogenetics and Evolution 53 (2009) 463–478 Although Turlin (2005, 2007) proposes 22 species-groups, his re- Against this background, the aim of the study was to test the view, also based on adult morphology and life history, is still under monophyly of Charaxes and its putative subgroups within a way and incomplete. Turlin’s species-group categorization is not as phylogenetic hypothesis reconstructed from molecular data of five widely accepted and operational as Van Someren’s (1969–1975) gene regions. We also investigated the evolutionary relatedness of and Henning’s (1989) species-groups hypotheses. We therefore the Charaxes species-groups in Africa and how they naturally relate adopt van Someren (and Henning’s) Charaxes species-group cate- to the species on other continents. The position of Charaxes among gorization for this study. Using this putative species-group catego- its two Africa sister candidates (Palla and Euxanthe) and its closest rization, the number of members in a species-group ranges from morphological sister groups (Polyura) were examined in this study. one (for four subgroups – Hadrianus, Zingha, Jahlusa, and Nichetes) Using the proposed phylogenetic hypothesis, we also estimated the to over 50 (in Etheocles). In the absence of a robust phylogenetic times of the major splits in Charaxes and related these divergence hypothesis, these traditional morphological hypotheses represent times with external factors that might have contributed to the tentative phenetic relationships of Charaxes species in Africa. How- diversification of the genus. Finally a zoogeographic hypothesis ever, the lack of discretionary power of phenetic analyses to distin- and probable events that might have led to the wide colonization guish between phylogenetically uninformative traits inherited and/or dispersal of the Charaxes in other continents were from an ancestor (plesiomorphies) and traits that evolved anew investigated using a dispersal–vicariance analysis (Ronquist, after divergence (synapomorphies) makes them liable to mislead. 1997). The field of molecular systematics has grown significantly with- in the last decade with an advanced battery of molecular markers. Characteristic of this development is an increase in confidence, 2. Materials and methods precision and accuracy of hypotheses used for testing the mono- phyly or otherwise of putative species-groups (Brooks et al., 2.1. Laboratory protocols 2007). Using these improved technologies and advancements in molecular systematics, Charaxes and its putative sister taxa are Selection of taxa for the study was based on available taxo- being recovered and resolved as a distinctive clade (Charaxinae) nomic information on the Charaxes species-group (Ackery et al., in various higher level butterfly systematic studies (e.g. Brower, 1995; Larsen, 2005; Williams, 2008). As ingroups, the exemplar 2000; Wahlberg et al., 2003; Freitas and Brown, 2004; Peña species were selected such that they represented all known ‘infor- et al., 2006; Peña and Wahlberg, 2008). Charaxinae consist of mal’ species-groups of Charaxes in Africa (a total of 125 specimens 350 species and 20 genera worldwide. Charaxes alone makes up of 83 species). We also included as ingroups all known species of over 70% of the species in the subfamily Charaxinae. Two genera the two Charaxinae genera (Euxanthe and Palla) in Africa, three of (Palla Hübner, 1819 and Euxanthe Hübner, 1819) also placed in ca. 30 Oriental Charaxes and two exemplar species of Polyura. Out- Charaxinae are found exclusively in the Afrotropics. The remaining groups were selected to include other members of Charaxinae 17 genera (comprising 125 species) occur mainly in the Neotrop- which are putatively closely related to Charaxes. The trees were ical region, with a few genera being found in the Oriental and Aus- rooted with two species of Satyrinae (Bicyclus anynana and Morpho tralasian regions. The relationships of the Charaxinae genera have helenor) and one species of Calinaginae (Calinaga buddha). Individ- not been the focus of any major study, although Peña and Wahl- uals of the selected taxa were collected from the field either by the berg (2008) sampled single exemplar species of almost all of the authors or through collaborative effort with other collectors and genera in their study on
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