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An Integrative Taxonomic Revision of the Cape Verdean Skinks (Squamata, Scincidae)

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An Integrative Taxonomic Revision of the Cape Verdean Skinks (Squamata, Scincidae) Zoologica Scripta An integrative taxonomic revision of the Cape Verdean skinks (Squamata, Scincidae) AURE´ LIEN MIRALLES*, RAQUEL VASCONCELOS*, ANA PERERA,DAVID J. HARRIS &SALVADOR CARRANZA Submitted: 12 March 2010 Miralles, A., Vasconcelos, R., Perera, A., Harris, D. J. & Carranza, S. (2011). An integra- Accepted: 15 September 2010 tive taxonomic revision of the Cape Verdean skinks (Squamata, Scincidae). — Zoologica doi:10.1111/j.1463-6409.2010.00453.x Scripta, 40, 16–44. A comprehensive taxonomic revision of the Cape Verdean skinks is proposed based on an integrative approach combining (i) a phylogenetic study pooling all the previously pub- lished molecular data, (ii) new population genetic analyses using mitochondrial and nuclear data resulting from additional sampling, together with (iii) a morphological study based on an extensive examination of the scalation and colour patterns of 516 live and museum spec- imens, including most of the types. All Cape Verdean species of skinks presently recogni- sed, formerly regarded as members of the genera Mabuya Fitzinger, 1826 and Macroscincus Bocage, 1873 are considered as members of the Cape Verdean endemic genus Chioninia Gray, 1845. The new phylogeny and networks obtained are congruent with the previously published phylogenetic studies, although suggesting older colonization events (between 11.6 and 0.8 Myr old), and indicate the need for taxonomic changes. Intraspecific diversity has been analysed and points to a very recent expansion of Chioninia delalandii on the southern islands and its introduction on Maio, to a close connection between Chioninia stangeri island populations due to Pleistocene sea-level falls and to a generally low haplo- typic diversity due to the ecological and geological characteristics of the archipelago. Three new consistent morphological synapomorphies supporting two of the four main clades of the genus have been identified. The complex taxonomic status of Euprepes fogoen- sis O’Shaughnessy, 1874 has been resolved and a lectotype has been designated for this species; Chioninia fogoensis nicolauensis (Schleich, 1987) is elevated to species rank, whereas Chioninia fogoensis antaoensis (Schleich, 1987) is now regarded as a junior subjective syno- nym of C. fogoensis. Additionally, one new subspecies of Chioninia vaillanti and two of Chioninia spinalis are described (Chioninia vaillanti xanthotis ssp. n., Chioninia spinalis santia- goensis ssp. n. and Chioninia spinalis boavistensis ssp. n.) and a lectotype has been designated for Mabuia spinalis Boulenger, 1906. Finally, an identification key for the Chioninia species is presented. Corresponding author: Salvador Carranza, Institute of Evolutionary Biology (CSIC-UPF), Pas- seig de la Barceloneta 39-47, 08003 Barcelona, Spain. E-mail: [email protected] Aure´lien Miralles, Department of Evolutionary Biology, Zoological Institute, Technical University of Braunschweig, Spielmannstrasse 8, 38106 Braunschweig, Germany. E-mail: miralles. [email protected] Raquel Vasconcelos, CIBIO, Centro de Investigac¸a˜o em Biodiversidade e Recursos Gene´ticos, Campus Agra´rio de Vaira˜o, R. Padre Armando Quintas, 4485-661 Vaira˜o, Portugal; Departamento de Biologia, Faculdade de Cieˆncias da Universidade do Porto, R. do Campo Alegre, s ⁄ n, 4169-007 Porto, Portugal; Institute of Evolutionary Biology (CSIC-UPF), Passeig de la Barceloneta 39-47, 08003 Barcelona, Spain. E-mail: [email protected] Ana Perera and D. James Harris, CIBIO, Centro de Investigac¸a˜o em Biodiversidade e Recursos Gene´ticos, Campus Agra´rio de Vaira˜o, R. Padre Armando Quintas, 4485-661 Vaira˜o, Portugal. E-mails: [email protected], [email protected] *These authors contributed equally to this work. Introduction issue of empirically testing species boundaries has been Definition of species concepts is one of the most inten- given little attention (Sites & Marshall 2003; De Queiroz sively debated subjects in evolutionary biology, but the 2007). The issue of species delimitation has long been 16 ª 2010 The Authors d Zoologica Scripta ª 2010 The Norwegian Academy of Science and Letters, 40, 1, January 2011, pp 16–44 A. Miralles et al. d Integrative taxonomy of the Cape Verdean skinks confused with that of species conceptualization, leading to tschudii, described from the Peruvian Amazonia (see Miral- a half century of controversy concerning both the defini- les et al. 2009)] and Chioninia Gray, 1845 exclusive to the tion of the species category and methods for inferring the Cape Verdean clade (Mausfeld et al. 2002; although see boundaries and numbers of species (Mayr 1970; Mayden Jesus et al. 2005 and Whiting et al. 2006). 1997; Mishler & Theriot 2000; De Queiroz 2007). The The Cape Verde Islands constitute one of the four oce- practical issue of delimiting species boundaries is neverthe- anic archipelagos of the Macaronesian biogeographical less of central importance to evolutionary biology, as it region, situated approximately 500 km off the Senegal defines the limits within or across which evolutionary pro- coast. It is a volcanic archipelago with 10 islands and vari- cesses operate. Recently, intellectual progress in this field ous islets, ranging from 26 to 6 Myr old (Fig. 1). Before has been achieved in two ways: firstly, through the Gen- this study, 13 extant native reptile species were recognised eral Lineage Species Concept it is now widely understood (see Joger 1993; Arnold et al. 2008), all endemic to the that almost all species concepts agree in defining that spe- archipelago. These belong to three genera: the Hemidacty- cies are population-level evolutionary lineages, and that lus and Tarentola geckos and the Chioninia skinks. Within refer to diagnostic characters of these lineages that become the latter, six extant species were recognised by Joger recognizable in a variable order and after different inter- (1993): Chioninia delalandii (Dume´ril & Bibron, 1839), vals of time; secondly, there is a vivid and fruitful discus- Chioninia vaillanti (Boulenger, 1887), Chioninia fogoensis sion about the novel concept of integrative taxonomy (O’Shaughnessy, 1874), Chioninia geisthardti (Joger, 1993), (sensu Dayrat 2005). This concept rejects the superiority of Chioninia stangeri (Gray, 1845), Chioninia spinalis (Bouleng- any particular set of characters (morphological, behaviour- er, 1906) and the extinct Chioninia coctei (Dume´ril & al, molecular, etc.) over others during the process of Bibron, 1839). Although the phylogenetic relationships recognizing and diagnosing species, and advocates the within Chioninia have been investigated previously (Brehm combined and integrated use of various such methods. et al. 2001; Brown et al. 2001; Carranza et al. 2001), all However, the development of this concept is ongoing, so these studies stressed that a review of the systematics of there is still no clear and consensual definition of what the Cape Verdean skinks was needed. For instance, ‘Ma- ‘integrative taxonomy’ is (see Padial et al. 2010). Among buya’ spinalis formed a complex assemblage of distinct lin- the proposed work protocols, there are those that seek for eages, and ‘Mabuya’ fogoensis was paraphyletic. Therefore, congruence among data sets as a main criterion for delim- the last revisions published (Mertens 1955; Schleich 1987) iting species boundaries (Cardoso et al. 2009) and those are now largely obsolete. Given the new data about the that argue that differences in a single marker are sufficient phylogenetic relationships of the group, its evolutionary (Padial et al. 2009). Regrettably, papers dealing with inte- history needs to be recounted. Also, as effective conserva- grative taxonomy have been until now theoretical, none of tion measures depend largely on a good knowledge of the them having yet applied such protocols to achieve concrete taxonomy and phylogeny of the species (Mace 2004), this taxonomic revisions. Therefore, in this article, a prag- study is essential for the assessments and future manage- matic, standardized and repeatable protocol of species ment of the Chioninia skinks. boundaries delimitation has been defined, which integrates In this work, a comprehensive review of the Cape Ver- the results of phylogenetic, population genetic analyses, dean skinks is proposed based on an integrative taxonomic and morphological studies, putting it into pratice to approach, combining (i) a new phylogenetic study pooling propose a comprehensive taxonomic revision of the Cape all the molecular data previously published for this genus Verdean skinks of the genus Chioninia. to estimate divergence times and island colonization pat- For a long time, the genus Mabuya Fitzinger, 1826 was terns; (ii) new population genetic analyses using mitochon- regarded as a very large pantropical group of lizards, drial (cyt b, cytochrome b) and nuclear data (RAG2, including more than 110 species occurring in tropical recombination activating gene), resulting from broad sam- areas of Africa, Asia and the New World (Greer & Broad- pling to examine intraspecific diversity; (iii) an extensive ley 2000). Then, during the last decade, several phyloge- examination of the morphology and colour patterns of live netic analyses (Mausfeld et al. 2002; Carranza & Arnold animals and specimens housed at museums (including 2003) identified distinct geographic monophyletic lineages most of the types) to reassess the systematics of the group. supporting its breakup into four genera. As a consequence, Mabuya sensu stricto is now a term restricted to
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