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Forgotten in the Ocean: Systematics, Biogeography and Evolution of the Trachylepis Skinks of the Socotra Archipelago

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Forgotten in the Ocean: Systematics, Biogeography and Evolution of the Trachylepis Skinks of the Socotra Archipelago Zoologica Scripta Forgotten in the ocean: systematics, biogeography and evolution of the Trachylepis skinks of the Socotra Archipelago R. SINDACO,M.METALLINOU,F.PUPIN,M.FASOLA &S.CARRANZA Submitted: 30 August 2011 Sindaco, R., Metallinou, M., Pupin, F., Fasola, M. & Carranza, S. (2012). Forgotten in the Accepted: 2 February 2012 ocean: systematics, biogeography and evolution of the Trachylepis skinks of the Socotra doi:10.1111/j.1463-6409.2012.00540.x Archipelago. —Zoologica Scripta, 41, 346–362. The Socotra Archipelago, in the north-west Indian Ocean, is considered to be one of the most remote and most biodiversity rich and distinct islands in the world. Often referred to as the ‘Galapagos of the Indian Ocean’, it was designated a UNESCO World Heritage Natural site in 2008. Despite having a very rich and bizarre fauna and flora with a high level of ende- micity at both species and generic levels, the taxonomy of most of the groups is still not clear, and their origin and evolution remain unknown. Reptiles constitute the most relevant verte- brate fauna of the Socotra Archipelago, with 90% of the 30 species and 45% of the 12 genera being found nowhere else in the world. The skinks of the endemic species Trachylepis socotr- ana are the only reptile species in the Archipelago distributed across all four islands (Socotra, Darsa, Samha and Abd Al Kuri). Although the species is very well known from Socotra Island, it was not discovered on Samha until 1999 and on Darsa until 2000, whereas only a few citations and one single Museum specimen exist for the population from Abd Al Kuri. To clarify the systematics, biogeography and evolution of Trachylepis socotrana, we assembled a dataset for Mabuya sensu lato including 904 base pairs (bp) of sequence (392 bp from the 12S and 512 from the 16S rRNA mitochondrial genes) for 115 individuals, including specimens of T. socotrana from all four island populations, numerous representatives of the genus Trachylepis from the Middle East, Africa and Madagascar, plus some individuals from each of the other three genera of Mabuya sensu lato (Chioninia, Eutropis and Mabuya). The results of the phylogenetic analyses indicate that, contrary to what was previously thought, members of the genus Trachylepis have colonized the Socotra Archipelago in two independent events, with the first giving rise to the populations from Socotra, Samha and Darsa and the second to the Trachylepis from Abd Al Kuri Island. According to the calibrations, both colo- nization events occurred within the last fourteen million years, when the Socotra Archipelago had already drifted away from Arabia, thus ruling out vicariance. Both morphological and genetic data show that the Trachylepis from Abd Al Kuri is a distinct taxon, which is herein described as a new species belonging to the T. brevicollis species complex. On the basis of this evidence, the terrestrial herpetofauna from Abd Al Kuri is composed exclusively of endemic species (one of which, the gecko Pristurus abdelkuri, was introduced into some parts of Socotra). Corresponding author: Salvador Carranza, Institute of Evolutionary Biology (CSIC-UPF), Passeig Marı´tim de la Barceloneta, 37-49, E-08003 Barcelona, Spain. E-mail: salvador.carranza@ ibe.upf-csic.es Roberto Sindaco, Museo Civico di Storia Naturale, via San Francesco di Sales 188, I-10022 Carmagnola, Italy. E-mail: [email protected] Margarita Metallinou, Institute of Evolutionary Biology (CSIC-UPF), Passeig Marı´tim de la Barce- loneta 39-47, 08003 Barcelona, Spain. E-mail: [email protected] Fabio Pupin, Museo Tridentino di Scienze Naturali, Via Calepina 14, I-38122 Trento, Italy. E-mail: [email protected] Mauro Fasola, Dipartimento di Biologia Animale, Universita` di Pavia, Via Ferrata 1, I-27100 Pavia, Italy. E-mail: [email protected] Salvador Carranza, Institute of Evolutionary Biology (CSIC-UPF), Passeig Marı´tim de la Barcelon- eta 39-47, 08003 Barcelona, Spain. E-mail: [email protected] 346 ª 2012 The Authors d Zoologica Scripta ª 2012 The Norwegian Academy of Science and Letters, 41, 4, July 2012, pp 346–362 Sindaco et al. d The Trachylepis skinks of the Socotra Archipelago Introduction 2004; Bosworth et al. 2005). Tectonic activity in the Red The Socotra Archipelago comprises four islands of conti- Sea ⁄ Gulf of Aden region during the Oligocene produced nental origin situated in the north-west Indian Ocean, arching and block faulting along the axis of the embryo near the Gulf of Aden (Fig. 1). It is considered one of the Gulf, thereby giving rise to the Gulf of Aden and the most remote and most biodiversity rich and distinct archi- east–west faults of southern Arabia (Laughton 1966). Sub- pelagos in the world. Termed the ‘Galapagos of the Indian sequent sub-crustal movements also produced forces that Ocean’, it was designated a UNESCO World Heritage both carried the Arabian block north–north-east and Natural site in 2008 (Van Damme 2009). The easternmost rotated it anticlockwise, thus producing a line of parting and largest of these four islands is also called Socotra and, between the African and Arabian continental blocks that at just 3625 km2, comprises about 95% of the total land- passed between Socotra and the Hallaniyat Islands (for- mass of the archipelago. It is also the most ecologically, merly Kuria Muria Islands) in south-west Oman (Fig. 1). geographically and biologically diverse. Abd Al Kuri, the These tectonic movements marked the onset of the rifting second largest (133 km2) and westernmost island of the between Arabia and Somalia in the late Oligocene ⁄ early archipelago, lies about 105 km to the west of Socotra and Miocene (30–17.6 mya). This period, also known as the 100 km east of the Horn of Africa. The other two islands, syn-rift time, was followed by the postrift time, which was namely Darsa (16 km2) and Samha (40 km2), also known characterized by continental break-up and oceanic spread- as ‘The Brothers’, are much smaller and are situated 36 ing at 17.6 mya in the eastern part of the Gulf of Aden and 50 km, respectively, to the west of Socotra. Two and increased the distance between the Socotra Archipel- rocky guano islets (Ka’l Fir’awn and Sabuniyah) situated ago and Arabian mainland (Laughton 1966; Bosworth 20 km north of Abd Al Kuri and 20 km north-east et al. 2005; Autin et al. 2010). of Socotra, respectively, are apparently devoid of As the Socotra Island is separated from Samha and herpetofauna. Darsa by shallow seas, it has been suggested that they The Socotra Archipelago rests on a shelf platform that were connected during the sea-level changes that occurred is attached to the Horn of Africa. Plate tectonic recon- in the Pleistocene. In contrast, Abd Al Kuri is separated structions indicate that, prior to the rifting of the Gulf of from the other islands of the archipelago and from the Aden, the Socotra shelf and its islands were located adja- Horn of Africa by depths of between 200 and 1000 m, cent to the Dhofar region of Southern Oman, an interpre- which, therefore, exceed Pleistocene sea-level changes tation well-supported by comparisons of the Mesozoic and (Cheung & DeVantier 2006). Tertiary successions in these two areas (Laughton 1966; This complex geological history, which includes a long Laughton et al. 1970; Samuel et al. 1997; Fleitmann et al. period of isolation, together with its topography and its Fig. 1. Map showing the geographical situation of the Socotra Archipelago. ª 2012 The Authors d Zoologica Scripta ª 2012 The Norwegian Academy of Science and Letters, 41, 4, July 2012, pp 346–362 347 The Trachylepis skinks of the Socotra Archipelago d Sindaco et al. different microclimates form the basis of the high biodi- The genus Trachylepis is one of the four units into which versity and endemism of the Socotra Archipelago. For the genus Mabuya, one of the largest genera of the Scinci- example, 37% of Socotra’s 825 plant species, 90% of its dae family, was split based on molecular and distributional 30 reptile species and 95% of its more than 100 land data (Mausfeld et al. 2002). The other three genera are snail species are not found anywhere else in the world Chioninia (Cape Verde Archipelago), Eutropis (Asian spe- (Sindaco et al. 2009; Van Damme 2009; Razzetti et al. cies) and Mabuya (South and Central America and the 2011). Endemism is especially high at the generic level, Caribbean, except for Trachylepis atlantica from the island with 75% of the land snail genera, 41% of the reptile of Fernando de Noronha, Brazil, and the enigmatic genera and 3.5% of the plant genera being unique to the T. tschudii described from the Peruvian Amazonas; see archipelago. Despite the richness and importance of Miralles et al. 2009a). Although these four genera have Socotra’s biodiversity, little is known about the phylog- been accepted in the latest taxonomic works (Mausfeld & eny, evolution and biogeography of most of the islands’ Schmitz 2003; Miralles et al. 2009a,b; Miralles & Carranza species, and many of the groups, therefore, need taxo- 2010; Miralles et al. 2011), the phylogenetic affinities of a nomic revision (Sindaco et al. 2009; Van Damme 2009; fifth unnamed clade formed by a few species from the Razzetti et al. 2011). A clarification of the systematics and Middle East are still unresolved (Carranza & Arnold 2003; a better understanding of the phylogeographic patterns Miralles & Carranza 2010). According to Mausfeld & and genetic population structure in areas of conservation Schmitz (2003), the Middle East clade is part of Trachyl- concern, such as islands, are therefore crucial to delimit epis. However, the monophyly of Trachylepis has never evolutionarily significant units and design efficient conser- been properly tested; therefore, inclusion of the Middle vation measures.
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