Multilocus Phylogeny and a New Classification for African, Asian and Indian Supple and Writhing Skinks (Scincidae: Lygosominae)

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Multilocus Phylogeny and a New Classification for African, Asian and Indian Supple and Writhing Skinks (Scincidae: Lygosominae) Zoological Journal of the Linnean Society, 2019, XX, 1–30. With 5 figures. Downloaded from https://academic.oup.com/zoolinnean/advance-article-abstract/doi/10.1093/zoolinnean/zlz001/5428841 by Oklahoma State University (GWLA) user on 08 April 2019 Multilocus phylogeny and a new classification for African, Asian and Indian supple and writhing skinks (Scincidae: Lygosominae) ELYSE S. FREITAS1*, ANIRUDDHA DATTA-ROY2,3, PRAVEEN KARANTH2, L. LEE GRISMER4 and CAMERON D. SILER1 1Sam Noble Oklahoma Museum of Natural History and Department of Biology, University of Oklahoma, 2401 Chautauqua Ave, Norman, OK 73072–7029, USA 2Centre for Ecological Sciences, Indian Institute of Science, Bangalore 560 012, India 3School of Biological Sciences, National Institute of Science Education and Research, Bhubaneswar, 752050, Odisha, India 4Department of Biology, La Sierra University, Riverside, California, USA Received 10 May 2018; revised 6 December 2018; accepted for publication 24 December 2018 The genera Lepidothyris, Lygosoma and Mochlus comprise the writhing or supple skinks, a group of semi-fossorial, elongate-bodied skinks distributed across the Old World Tropics. Due to their generalized morphology and lack of diagnostic characters, species- and clade-level relationships have long been debated. Recent molecular phylogenetic studies of the group have provided some clarification of species-level relationships, but a number of issues regarding higher level relationships among genera still remain. Here we present a phylogenetic estimate of relationships among species in Lygosoma, Mochlus and Lepidothyris generated by concatenated and species tree analyses of multilocus data using the most extensive taxonomic sampling of the group to date. We also use multivariate statistics to examine species and clade distributions in morpho space. Our results reject the monophyly of Lygosoma s.l., Lygosoma s.s. and Mochlus, which highlights the instability of the current taxonomic classification of the group. We, therefore, revise the taxonomy of the writhing skinks to better reflect the evolutionary history of Lygosoma s.l. by restricting Lygosoma for Southeast Asia, resurrecting the genus Riopa for a clade of Indian and Southeast Asian species, expanding the genus Mochlus to include all African species of writhing skinks and describing a new genus in Southeast Asia. ADDITIONAL KEYWORDS: Africa – India – Lamprolepis – Lepidothyris – Lygosoma – Mochlus – Riopa – Southeast Asia – taxonomy. INTRODUCTION relationships across many clades in the family remain poorly resolved (Pyron et al., 2013; Skinner et al., 2013; The lizard family Scincidae is the most species-rich Barley et al., 2015a; Lambert et al., 2015; Zheng & family of squamate reptiles. Skinks are ecologically and morphologically diverse, with more than 1600 taxa Wiens, 2016), However, with the continued growth currently recognized (Uetz et al., 2019) as occurring in available genetic data and increased taxonomic in tropical and temperate zones on all continents sampling in molecular systematic studies of various excluding Antarctica, as well as on many oceanic clades, research over the last decade has contributed islands (Greer, 1970a; Vitt & Caldwell, 2013). Despite greatly to an improved understanding of the diversity of this high diversity, inter- and intrageneric phylogenetic scincid lizards (e.g. Linkem et al., 2011; Siler et al., 2011; Brandley et al., 2012; Datta-Roy et al., 2012; Sindaco et al., 2012; Skinner et al., 2013; Datta-Roy et al., *Corresponding author. E-mail: [email protected] 2014; Barley et al., 2015a; Pinto-Sánchez et al., 2015; [Version of record, published online on 5 April 2019; http://zoobank.org urn:lsid:zoobank. Karin et al., 2016; Klein et al., 2016; Erens et al., 2017). org:pub:8AA92D8A-A294-4B62-9A75-5CA4534CFCBC] Additionally, this nascent body of work has resulted in © 2019 The Linnean Society of London, Zoological Journal of the Linnean Society, 2019, XX, 1–30 1 2 E. S. FREITAS ET AL. Downloaded from https://academic.oup.com/zoolinnean/advance-article-abstract/doi/10.1093/zoolinnean/zlz001/5428841 by Oklahoma State University (GWLA) user on 08 April 2019 a dramatic increase in the discovery of morphologically et al., 2018; Uetz et al., 2019). Genera closely allied to cryptic lineages (e.g. Daniels et al., 2009; Linkem et al., Lygosoma are Mochlus, consisting of 15 species found in 2010; Chapple et al., 2011; Heideman et al., 2011; Siler semi-arid regions across central and subtropical southern et al., 2011, 2012, 2014, 2016, 2018; Kay & Keogh, 2012; Africa, and Lepidothyris, consisting of three species Barley et al., 2013; Davis et al., 2014, 2016; Geheber et al., found in forested regions of Central Africa (Greer, 1977; 2016; Heitz et al., 2016; Medina et al., 2016; Busschau Wagner et al., 2009; Uetz et al., 2019). Historically, the et al, 2017; Conradie et al., 2018; Karin et al., 2018; taxonomic status of these three genera has been debated Pietersen et al., 2018). In spite of all these efforts, there extensively, with species in Mochlus and Lepidothyris remain many lingering taxonomic and phylogenetic often included in Lygosoma (e.g. Boulenger, 1887; Greer, challenges in the family, possibly none more so than in 1977; see taxonomic history of the group below), and the large and diverse subfamily Lygosominae. recent phylogenetic analyses suggest that Lygosoma is One of three subfamilies recognized widely in the paraphyletic with respect to both genera (Pyron et al., lizard family Scincidae (Greer, 1970a; Pyron et al., 2013; 2013; Datta-Roy et al., 2014). Therefore, from here on Skinner et al., 2013; Lambert et al., 2015; Karin et al., out, we refer to the 49 species represented by these three 2016; Linkem et al., 2016; Zheng & Wiens, 2016; but see genera collectively as Lygosoma s.l., whereas, we refer an alternative, less widely accepted classification in: to the 31 species in the genus Lygosoma (as currently Hedges & Conn, 2012; Hedges, 2014; Uetz et al., 2018), recognized) as Lygosoma s.s. the Lygosominae contains approximately 1354 species Although Greer (1977) found all members of Lygosoma (estimated from: Uetz et al., 2019) and represents, s.l. to be united by osteological characteristics of the currently, the most species-rich radiation of scincid secondary palate, morphology has offered few clues to lizards, with a broad, global distribution (Greer, 1970a; the phylogenetic relationships of species and clades in Honda et al., 2000; Skinner et al., 2011). The radiation the group, which has resulted in considerable taxonomic likely began diversifying 100.6–63.6 Mya, during the Late confusion regarding the status of species and genera Cretaceous to Early Palaeocene (Skinner et al., 2011). (e.g. Broadley, 1966; Greer, 1977). Known as supple or Extant lygosomine genera exhibit a rich biogeographical writhing skinks, species have been allocated to Lygosoma history, with evidence for historical transoceanic s.l. generally on the basis of their semi-fossorial ecology, dispersal in some lineages (Carranza & Arnold, 2003; head scale patterns well-developed eyelids, elongate Honda et al., 2003; Rocha et al., 2006; Linkem et al., bodies and short fore- and hind limbs that do not meet 2013; Skinner et al., 2013; Karin et al., 2016). Many when appressed (Smith, 1935; Mittleman, 1952; Greer, genera have been the subject of recent phylogenetic 1977; Geissler et al., 2011; Geissler, Hartmann & Neang, studies, including Afroablepharus and Panaspis (Medina 2012). All species are pentadactyl with the exception of et al., 2016), Eutropis (Datta-Roy et al., 2012; Barley Lygosoma lineatum Gray, 1839, which has tetradactyl et al., 2013, 2015a), Lygosoma (Datta-Roy et al., 2014), fore-limbs (Greer, 1977). Colour and pigmentation Mabuya (Hedges & Conn, 2012; Pinto-Sánchez et al., patterns vary within and between species (Wagner 2015), Sphenomorphus (Linkem et al., 2011), Trachylepis et al., 2009). However, beyond these generalizations, (Sindaco et al., 2012) and Tytthoscincus (Grismer species exhibit diverse body forms that range from et al., 2018a). Although these studies have increased moderately large (e.g. Lygosoma kinabatanganense the understanding of diversity and relationships Grismer, Quah, Duzulkafly & Yambun, 2018: snout– among these focal clades, they also have highlighted vent length [SVL] = 141 mm; L. haroldyoungi (Taylor, a number of phylogenetic and taxonomic issues that 1962): SVL = 148 mm; Mochlus sundevallii (Smith, remain unresolved. As taxonomy reflects our knowledge 1894): SVL = 140 mm) to small (e.g. L. frontoparietale of organisms in the tree of life (Vences et al., 2013), (Taylor, 1962): SVL = 41 mm; L. veunsaiense Geissler, resolving these conflicts is important for investigating Hartmann & Neang, 2012: SVL = 34 mm) and more a myriad of higher level questions, including studies robust with short limbs (e.g. M. brevicaudis Greer, of ecology, diversification, morphological evolution and Grandison & Barbault, 1985), to elongate and more conservation of imperilled species. gracile with small, slender limbs and shorter digits One prime example of unresolved taxonomic issues (e.g. L. quadrupes (Linnaeus, 1766)) (Broadley, 1966; among lygosomine skinks is the genus Lygosoma, which Greer, 1977; Geissler et al., 2011). As a result of this has a long and controversial history of uncertainty considerable diversity in body form, researchers have regarding species- and generic-level relationships. struggled to define morphological boundaries between Lygosoma Hardwicke
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