Multilocus phylogeny of Bornean Bent-Toed geckos (Gekkonidae: Cyrtodactylus) reveals hidden diversity, taxonomic disarray, and novel biogeographic patterns

Abstract

The gekkonid genus Cyrtodactylus is a highly diverse group of lizards (280 + species), which covers an expansive geographic range. Although this genus has been the focus of many taxonomic and molecular systematic studies, species on the Southeast Asian island of Borneo have remained understudied, leading to an unclear evolutionary history with cascading effects on taxonomy and biogeographic inferences. We assembled the most comprehensive multilocus Bornean dataset (one mitochondrial and three nuclear loci) that included 129 novel sequences and representatives from each known Cyrtodactylus species on the island to validate taxonomic status, assess species diversity, and elucidate biogeographic patterns. Our results uncovered a high proportion of cryptic diversity and revealed numerous taxonomic complications, especially within the C. consobrinus, C. malayanus, and C. pubisulcus groups. Comparisons of pairwise genetic distances and a preliminary species delimitation analysis using the Automatic Barcode Gap Discovery (ABGD) method demonstrated that some wide-ranging species on Borneo likely comprise multiple distinct and deeply divergent lineages, each with more restricted distributional ranges. We also tested the prevailing biogeographic hypothesis of a single invasion from Borneo into the Philippines. Our analyses revealed that Philippine taxa were not monophyletic, but were likely derived from multiple separate invasions into the geopolitical areas comprising the Philippines. Although our investigation of Bornean Cyrtodactylus is the most comprehensive to-date, it highlights the need for expanded taxonomic sampling and suggests that our knowledge of the evolutionary history, systematics, and biogeography of Bornean Cyrtodactylus is far from complete.

Phylogenetic partitioning of the third-largest vertebrate genus in the world, Cyrtodactylus Gray, 1827 (Reptilia; Squamata; Gekkonidae) and its relevance to taxonomy and conservation

“…These three clades correspond to 1) a Bornean radiation (С. baluensis, С. ingeri, and С. yoshii) sister to at least three southern Philippine taxa (С. annulatus, С. jambangan, and С. tautbatorum); 2) a single Philippine taxon (С. red-imiculus) sister to at least three Sundaic species (С. consobrinus, С. aurensis, and С. muluensis); and 3) an exclusively Philippine clade (С. agusanensis, С. gubaot, С. mamanwa (not in this study), С. philippinicus, and С. sumuroi). Worth noting, is that the topology inferred here differs from those recovered in previous studies that included multiple members of the group (Brennan et al 2017;Davis et al 2020;Nielsen and Oliver 2017;Siler et al 2010;Welton et al 2010a,b;Wood et al 2012), likely due to increased taxon sampling and the loci utilized. Though the relationships between Philippine and Sundaic taxa is unsurprising, the topology inferred from mitochondrial data indicates multiple dispersal events between the two faunal regions, yielding the Philippine assemblage of species paraphyletic.…”

“…Although its monophyly is well-supported (100/1.00), its relationships to other species groups are not. In a previous analysis (Davis et al 2019(Davis et al , 2020, some species of the malayanus group as constituted herein were nested within what is considered here as the well-supported (100/1.00) philippinicus group. However, the taxonomy of those phylogenies had a number of species (С. pubisulcus, С. cavernicolus, С. yoshii, С. malayanus, and С. consobrinus) occurring in multiple places throughout the tree rendering them polyphyletic and making comparisons with this tree not possible.…”

“…4): Cyrtodactylus tripuraensis (Agarwal et al 2014); С. pulchellus (Grismer et al 2012a(Grismer et al , 2014aQuah et al 2019;Wood et al 2020a); С. tuberculatus (Tallowin et al 2018); С. albofasciatus, С. deccanensis, and С. speciosus (Agarwal and Karanth 2015); С. pseudoquadrivirgatus (Luu et al 2017); С. pubisulcus (Davis et al 2019(Davis et al , 2020, and С. malayanus (Davis et al 2020). The non-monophyly of the latter species, however, may have to do with GenBank misidentifications and not mito-nuclear mismatch (Davis et al 2020).…”

Genetically diverse yet morphologically conserved: Hidden diversity revealed among Bornean geckos (Gekkonidae: Cyrtodactylus )

“…Genetic data demonstrated that many wide‐ranging taxa comprised genetically distinct groups, with many species being referred to as cryptic (Agarwal & Karanth, 2015; Agarwal et al, 2018; Grismer et al, 2012, 2014, 2016, 2018; Luu et al, 2016; Murdoch et al, 2019; Nazarov, Orlov, Sang, & Cuc, 2008, 2012; Nguyen et al, 2017; Oliver et al, 2012, 2018; Ziegler et al, 2010). These molecular‐based systematic studies have been instrumental in uncovering hidden diversity, but the Southeast Asian island of Borneo has only recently been investigated (Davis et al, 2019, 2020). Due to the prior lack of molecular genetic studies on Borneo, only 10 species of Cyrtodactylus are currently recognized, nine of which are endemic.…”

“…Although Borneo and Peninsular Malaysia shared a recent terrestrial connection (Sarr et al, 2019), Peninsular Malaysia has nearly four times the recognized Cyrtodactylus diversity (Grismer & Quah, 2019), which suggests that Bornean Cyrtodactylus diversity may be substantially higher. The recent studies targeting the diversity of Bornean Cyrtodactylus highlighted the high amount of diversity on the island with multiple undescribed cryptic lineages and high intraspecific genetic diversity (Davis et al, 2019, 2020).…”