Molecular Phylogenetics and Evolution 133 (2019) 166–175 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev An integrative study of island diversification: Insights from the endemic Haemodracon geckos of the Socotra Archipelago T ⁎ Karin Tamara, , Marc Simó-Riudalbasa, Joan Garcia-Portab, Xavier Santosc, Gustavo Llorented, Raquel Vasconcelosa,c, Salvador Carranzaa a Institute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta 37–49, 08003 Barcelona, Spain b CREAF, Cerdanyola del Vallès, Spain c CIBIO Research Centre in Biodiversity and Genetic Resources, InBIO, Universidade do Porto, Campus de Vairao, Rua Padre Armando Quintas, N° 7, 4485–661 Vairao, Portugal d Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals, Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Avda. Diagonal 643, 08028 Barcelona, Spain ARTICLE INFO ABSTRACT Keywords: The Socotra Archipelago in the Arabian Sea is considered one of the most geo-politically isolated landforms on In situ diversification earth and a center of endemism. The archipelago is located at the western edge of the Indian Ocean and com- Phenotypic diversification prises four islands: Socotra, Darsa, Samha, and Abd al Kuri. Here we provide an integrative study on Phylogeography Haemodracon geckos, the sole genus of geckos strictly endemic to the archipelago. The sympatric distribution of Body size Haemodracon riebeckii and H. trachyrhinus on Socotra Island provides a unique opportunity to explore evolu- Evolution tionary relationships and speciation patterns, examining the interplay between possible sympatric and allopatric Micro-habitat scenarios. We used molecular data for phylogenetic inference, species delimitation analyses, and to infer the diversification timeframe. Multivariate statistics were used to analyze morphological data. Ecological compar- isons were explored for macro-niches using species distribution models and observations were used for micro- habitat use. Haemodracon species exhibit great levels of intraspecific genetic diversity. Our calibration estimates revealed that Haemodracon diverged from its closest relative, the mainland genus Asaccus, in the Eocene, before the detachment of the archipelago. The two Haemodracon species diversified in situ on Socotra Island during the Middle Miocene, after the archipelago’s isolation, into the two reciprocally monophyletic recognized species. Their divergence is associated mostly with remarkable body size differences and micro-habitat segregation, with low levels of climatic and body shape divergences within their sympatric distributions. These results display how ecological, sympatric speciation, and allopatric speciation followed by secondary contact, may both have varying roles at different evolutionary phases. 1. Introduction interest (e.g., Schluter, 2000; Losos, 2009; Losos and Ricklefs, 2009; Nosil, 2012; see references therein). Historical, geographic, and environmental effects contribute to Islands are widely used to study evolutionary and ecological pat- current processes of diversification through various mechanisms, with terns as they have well-defined borders, they are relatively easy to both adaptive and non-adaptive components. On the one hand, ecolo- sample, and comprise simplified ecosystems with mostly well-known gical opportunity can induce diversification generating phenotypic di- geological histories (Woolfit and Bromham, 2005; Whittaker and vergence (Gavrilets and Losos, 2009; Losos and Ricklefs, 2009; Schluter, Fernandez-Palacios, 2007). These characteristics provide the ideal 2000; Stroud and Losos, 2016). On the other, allopatric processes can context to explore the role of adaptive and non-adaptive components in produce diversification not necessarily involving phenotypic and eco- diversifying insular groups (Losos and Ricklefs, 2009). Intra-island logical differentiation (Sharbel et al., 2000; Kuchta and Tan, 2005; speciation processes largely depend on island size, age, topography, Kozak and Wiens, 2007). Although adaptive and non-adaptive compo- isolation, and environmental heterogeneity to promote effective seg- nents have been identified in many diversifying groups, the interplay regation of populations by divergent natural selection pressures and between these two mechanisms has been and still is the focus of much micro-habitat specialization (horizontal and/or altitudinal), or by long- ⁎ Corresponding author. E-mail address: [email protected] (K. Tamar). https://doi.org/10.1016/j.ympev.2019.01.009 Received 8 June 2018; Received in revised form 7 January 2019; Accepted 7 January 2019 Available online 11 January 2019 1055-7903/ © 2019 Elsevier Inc. All rights reserved. K. Tamar et al. Molecular Phylogenetics and Evolution 133 (2019) 166–175 Arabian Peninsula 11 Arabian Socotra 70 Sea 633 9 22 40 56 66-68 Gulf of Aden 5 58 76 87 26 41 73 Horn of Africa 24 29 44 14 30 77 90 2-4 37 62 64 79-86 Socotra Archipelago 25 74 12 43 69 75 89 60 72 78 12.5 6-8 27 35,36 42 45-54 88 Samha 10 55 Socotra 21 Abd al Kuri 15 31 34 Darsa 61 71 13 59 17 38,39 65 23 32,33 57 16 18-20 28 Samha 1 Elevation (m) Darsa 0–375 375–750 750–1000 H. riebeckii 01020 km 1000–1125 H. trachyrhinus 1125–1500 12.0 53.0 53.5 54.0 54.5 Fig. 1. Localities of the material used in this study (i.e., genetic, morphological, and micro-habitat datasets) for Haemodracon riebeckii (red) and Haemodracon trachyrhinus (blue). Detailed lists of the datasets are presented in Table S1. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) term gene flow restriction (Whittaker and Fernandez-Palacios, 2007; However, in Pristurus and Haemodracon, these studies focused on the Whittaker et al., 2008; Losos and Parent, 2009; Kisel and Barraclough, deep phylogenetic structure among species and did not take into ac- 2010; Rosindell and Phillimore, 2011). count important components such as shallow genetic structure and The Socotra Archipelago in the Arabian Sea is regarded as one of the micro-habitat use that can shed light on the ongoing diversification most geo-politically isolated and biodiverse archipelagos in the world, processes. internationally recognized as a center of global vertebrate and plant In the present study, we use an integrative approach to investigate diversity and endemism (Olson and Dinerstein, 1998; Kier et al., 2009; diversification processes using Haemodracon geckos as a model. The Van Damme, 2009). The archipelago is an ancient continental frag- genus Haemodracon Bauer, Good & Branch, 1997 is endemic to the ment, which detached from the Arabian mainland and drifted to its Socotra Archipelago and is the only member of the family Phyllo- current position during the Oligocene-Miocene epochs (∼17–30 mil- dactylidae present on these islands. The genus comprises two nocturnal lion years ago [Mya]; Bosworth et al., 2005; Autin et al., 2013). It is sympatric species: Haemodracon riebeckii (Peters, 1882), the largest located at the western edge of the Indian Ocean and comprises four gecko species in the archipelago distributed on Socotra and Samha Is- islands (Fig. 1): Socotra, Darsa, Samha, and Abd al Kuri. Due to its lands; and Haemodracon trachyrhinus (Boulenger, 1899), much smaller geographic location at the intersect of the Indian, Arabian, and African and endemic to Socotra Island (Schätti and Desvoignes, 1999; Razzetti tectonic plates, the archipelago has experienced frequent tectonic and et al., 2011). Our general aims are to (i) study the intraspecific genetic seismic events, phases of partial submersion and interconnection diversity and phylogeography of Haemodracon using three mitochon- among the three former islands, pluvial and interpluvial periods and, drial and four nuclear markers, (ii) assess the time of divergence among although mainly arid, also stages of intense rainfall due to the Indian its genetic lineages and relate it to the geographic and climatic histories monsoons (Gupta et al., 2004; Cheung and De Vantier, 2006; Fleitmann of the archipelago, (iii) evaluate significant inter-specific size and shape et al., 2007). The complex geological and climatic histories of the ar- differences, and (iv) provide macro- and micro-ecological comparisons chipelago have created remarkably diverse topography, habitats, and between the species. By applying an integrative approach, we provide microclimates within the islands, especially within Socotra Island, the insights into the diversification process that shape evolutionary pat- largest and the most geographically, biologically, and ecologically di- terns on islands, especially on remote and under-studied regions as the verse of the four (Van Damme, 2009). Socotra Archipelago. Reptiles of the Socotra Archipelago constitute the vertebrate group with the highest endemicity at both the species and genus levels (Cheung and De Vantier, 2006). Recently, with the increasing avail- 2. Materials and methods ability of phylogenetic data, integrative studies on island diversification and dispersal mechanisms within the Socotra Archipelago have ex- 2.1. Molecular analyses emplified the complex evolutionary histories and micro-evolutionary processes of its reptile fauna (e.g., Sindaco et al., 2012; Gómez Díaz We sampled 46 specimens of the two recognized species of et al., 2012; Nagy et al., 2003; Garcia-Porta et al., 2016a,b; Vasconcelos Haemodracon from their entire distribution range