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A Molecular Phylogeny of Equatorial African Lacertidae, with the Description of a New Genus and Species from Eastern Democratic Republic of the Congo

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A Molecular Phylogeny of Equatorial African Lacertidae, with the Description of a New Genus and Species from Eastern Democratic Republic of the Congo Zoological Journal of the Linnean Society, 2011, 163, 913–942. With 7 figures A molecular phylogeny of Equatorial African Lacertidae, with the description of a new genus and species from eastern Democratic Republic of the Congo ELI GREENBAUM1*, CESAR O. VILLANUEVA1, CHIFUNDERA KUSAMBA2, MWENEBATU M. ARISTOTE3 and WILLIAM R. BRANCH4,5 1Department of Biological Sciences, University of Texas at El Paso, 500 West University Avenue, El Paso, TX 79968, USA 2Laboratoire d’Herpétologie, Département de Biologie, Centre de Recherche en Sciences Naturelles, Lwiro, République Démocratique du Congo 3Institut Superieur d’Ecologie pour la Conservation de la Nature, Katana Campus, Sud Kivu, République Démocratique du Congo 4Bayworld, P.O. Box 13147, Humewood 6013, South Africa 5Research Associate, Department of Zoology, Nelson Mandela Metropolitan University, Port Elizabeth, South Africa Received 25 July 2010; revised 21 November 2010; accepted for publication 18 January 2011 Currently, four species of the lacertid lizard genus Adolfus are known from Central and East Africa. We sequenced up to 2825 bp of two mitochondrial [16S and cytochrome b (cyt b)] and two nuclear [(c-mos (oocyte maturation factor) and RAG1 (recombination activating gene 1)] genes from 41 samples of Adolfus (representing every species), two species each of Gastropholis and Holaspis, and in separate analyses combined these data with GenBank sequences of all other Eremiadini genera and four Lacertini outgroups. Data from DNA sequences were analysed with maximum parsimony (PAUP), maximum-likelihood (RAxML) and Bayesian inference (MrBayes) criteria. Results demonstrated that Adolfus is not monophyletic: Adolfus africanus (type species), Adolfus alleni, and Adolfus jacksoni are sister taxa, whereas Adolfus vauereselli and a new species from the Itombwe Plateau of Democratic Republic of the Congo are in a separate lineage. Holaspis and Gastropholis were recovered in separate clades. Based on these molecular data, relatively substantial sequence divergence, and multiple morphological differences, we describe a new genus of lacertid for the lineage including A. vauereselli and the new Itombwe species. The recognition of this new, endemic genus underscores the conservation importance of the Albertine Rift, especially the Itombwe Plateau, a unique region that is severely threatened by unchecked deforestation, mining, and poaching.zoj_732 913..942 © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 913–942. doi: 10.1111/j.1096-3642.2011.00732.x ADDITIONAL KEYWORDS: Afromontane – Albertine Rift – conservation – endemism – Itombwe Plateau – lizard – systematics. INTRODUCTION low-elevation forests from Cameroon to Kenya), Adolfus alleni (montane moorlands of Kenya and Meadow and forest lizards of the lacertid genus Uganda), and Adolfus jacksoni and A. vauereselli, Adolfus are currently known from Central and which are both known from mid- to high-elevation East Africa, including Adolfus africanus (mid- to forests in countries surrounding the Albertine Rift (Spawls et al., 2002; Köhler et al., 2003). Adolfus are *Corresponding author. E-mail: [email protected] medium-sized (total size to 25.6 cm), relatively slim © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 913–942 913 914 E. GREENBAUM ET AL. lizards, and tend to be good climbers on standing and combination of morphology and mtDNA data that fallen timber, rocky walls, holes, and crevices (A. contradicted several findings of Mayer & Benyr (1994), africanus is also known to climb twiggy and herba- Harris et al. (1998) assigned the subfamily Eremiainae ceous plants), but tend to hunt on the ground (Arnold, (Szczerbak, 1975) to the Armatured Clade. 1989a, 1998; Spawls et al., 2002). Recent work on this More recent analyses of lacertids with mitochon- genus has included aspects of reproduction (A. jack- drial data have done little to clarify the position soni, Goldberg, 2009), endoparasites (A. jacksoni, of Adolfus in relation to other members of the Goldberg & Bursey, 2009), geographical distribution Equatorial African clade, or the ESE group as a (A. africanus, Köhler et al., 2003), and morphology whole. Although Fu (1998) recovered a monophyletic and colour pattern (A. jacksoni, Poblete, 2002). ‘African clade’ in a mitochondrial phylogeny of lac- The taxonomic status and affinities of the currently ertids, no members of the Equatorial African clade recognized species of Adolfus have changed consider- were included. Harris (1999) combined the mitochon- ably over time. The genus Adolfus was first proposed drial data of Fu (1998) and Harris et al. (1998) with by Sternfeld (1912) for the taxon Adolfus fridericianus, some new data to produce a phylogeny of Lacertidae, which was presumably in honour of Adolphus Freder- but support for the ESE clade (still recognized as ick, Duke of Mecklenburg, who led the German Central Eremiainae) was weak; two samples of Adolfus (A. Africa Expedition in 1907–08 when the specimens africanus and A. jacksoni) were not supported as were collected (Frederick, 1910). In his opus on the sister taxa. Fu (2000) published another phylogeny family Lacertidae, Boulenger (1920) considered A. of Lacertidae with six mitochondrial genes (4.7 kb of fridericianus to be a synonym of Algiroides africanus DNA data), with most trees supporting the mono- (= Algyroides africanus), a species he described in phyly of the ESE clade, but with the exception of 1906, and recognized Algiroides alleni, Lacerta jackso- three closely related genera (Nucras, Latastia,and nii (a species he described in 1899), and Lacerta Heliobolus), relationships amongst ESE genera were vauereselli. Based on morphological characters, Arnold unclear, and the monophyly of two samples of (1973) resurrected the genus Adolfus for A. africanus, Adolfus (A. jacksoni and A. vauereselli) was again A. alleni, and A. vauereselli, and noted a close relation- not supported. The latter two species of Adolfus were ship between this genus and Bedriagaia, Gastropholis, not recovered as monophyletic in a study focused on and L. jacksoni. In morphology-based parsimony and Australolacerta australis with mitochondrial data compatibility analyses, Arnold (1989a) transferred L. (Salvi, Bombi & Vignoli 2011). jacksoni to the genus Adolfus, synonymized Bedria- Mayer & Pavlicev (2007) published the first lacertid gaia with Gastropholis, recognized a clade called the phylogeny based on nuclear data [c-mos (oocyte matu- ‘Equatorial African group’ including Adolfus, Gastrop- ration factor) and RAG1 (recombination activating holis, and Holaspis (a well-supported clade recovered gene 1)], and recovered two clades within a well- in a later morphology-based phylogeny by Harris, supported ESE (Eremiainae) group: clade B1, mainly Arnold & Thomas, 1998), and discussed the problem- from sub-Saharan Africa, including Poromera, Nucras, atic relationship of Holaspis to the paraphyletic genus Latastia, Philochortus, Pseuderemias, Heliobolus, Adolfus; if the latter two genera were to be joined, Tropidosaura, Pedioplanis, Ichnotropis, and Meroles; Holaspis would have priority. Arnold (1989a, b) admit- and clade B2, mainly from the Saharo-Eurasian region, ted that Adolfus was poorly defined, and considered A. including Ophisops, Omanosaura, Acanthodactylus, jacksoni to be the most plesiomorphic member of the Eremias, Mesalina, Adolfus,andHolaspis, with the Equatorial African clade. In a more extensive morpho- latter two Central African genera as well-supported logical analysis of the entire family Lacertidae, Arnold sister taxa. Arnold, Arribas & Carranza (2007) (1989b) grouped the Equatorial African Clade with re-analysed the data sets of Harris et al. (1998) and Fu Lacerta jayakari (now Omanosaura jayakari), Lacerta (2000), and published yet another lacertid phylogeny australis (now Australolacerta australis) and several based on two mitochondrial genes [12S and cytochrome other genera (e.g. Tropidosaura, Poromera, Nucras)in b (cyt b)]. Although their main focus was not on the an ‘Ethiopian and advanced Saharo-Eurasian forms’ ESE group, they redefined the Eremiainae as the tribe (ESE) group, which was later included in an ‘Arma- Eremiadini, and placed the North African monotypic tured Clade’ (Afrotropical species plus Eremias, Acan- genus Atlantolacerta as the most basal member of the thodactylus, Mesalina,andOphisops) in recognition of Eremiadini. Pavlicev & Mayer (2009) criticized the the members’ unique supporting structure of the male data set of the latter study as ‘relatively short mito- hemipenis (Arnold, 1986a, 1998; Harris et al., 1998). chondrial sequences when all taxa are considered’, Mayer & Benyr (1994) used an albumin-based rejected the tribe Eremiadini (instead recognizing it as analysis of most lacertid genera to imply paraphyly of subfamily Eremiadinae), but confirmed the placement the ESE group, with some of the Saharo-Eurasian of Atlantolacerta as the most basal member of the genera grouping with European lacertids. Based on a group. Hipsley et al. (2009) used mitochondrial and © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 913–942 PHYLOGENY OF EQUATORIAL AFRICAN LACERTIDAE 915 Table 1. Primer sequences used in this study Name Source Sequence Gene 16SA-L Palumbi et al. (1991) 5′-CGCCTGTTTATCAAAAACAT-3′ 16S 16SB-H Palumbi et al. (1991) 5′-CCGGTCTGAACTCAGATCACGT-3′ 16S CytbF700 Bauer et al. (2007) 5′-CTTCCAACACCAYCAAACATCTCAGCATGATGAAA-3′ cyt b CytbR700
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