Molecular evidence for ten species and Oligo-Miocene vicariance within a nominal Australian gecko species (Crenadactylus ocellatus, Diplodactylidae)

Abstract

BackgroundMolecular studies have revealed that many putative 'species' are actually complexes of multiple morphologically conservative, but genetically divergent 'cryptic species'. In extreme cases processes such as non-adaptive diversification (speciation without divergent selection) could mask the existence of ancient lineages as divergent as ecologically and morphologically diverse radiations recognised as genera or even families in related groups. The identification of such ancient, but cryptic, lineages has important ramifications for conservation, biogeography and evolutionary biology. Herein, we use an integrated multilocus genetic dataset (allozymes, mtDNA and nuclear DNA) to test whether disjunct populations of the widespread nominal Australian gecko species Crenadactylus ocellatus include distinct evolutionary lineages (species), and to examine the timing of diversification among these populations.ResultsWe identify at least 10 deeply divergent lineages within the single recognised species Crenadactylus ocellatus, including a radiation of five endemic to the Kimberley region of north-west Australia, and at least four known from areas of less than 100 km2. Lineages restricted to geographically isolated ranges and semi-arid areas across central and western Australia are estimated to have began to diversify in the late Oligocene/early Miocence (~20-30 mya), concurrent with, or even pre-dating, radiations of many iconic, broadly sympatric and much more species-rich Australian vertebrate families (e.g. venomous snakes, dragon lizards and kangaroos).ConclusionsInstead of a single species, Crenadactylus is a surprisingly speciose and ancient vertebrate radiation. Based on their deep divergence and no evidence of recent gene flow, we recognise each of the 10 main lineages as candidate species. Molecular dating indicates that the genus includes some of the oldest vertebrate lineages confounded within a single species yet identified by molecular assessments of diversity. Highly divergent allopatric lineages are restricted to putative refugia across arid and semi-arid Australia, and provide important evidence towards understanding the history and spread of the Australian arid zone, suggesting at a minimum that semi-arid conditions were present by the early Miocene, and that severe aridity was widespread by the mid to late Miocene. In addition to documenting a remarkable instance of underestimation of vertebrate species diversity in a developed country, these results suggest that increasing integration of molecular dating techniques into cryptic species delimitation will reveal further instances where taxonomic conservatism has led to profound underestimation of not only species numbers, but also highly significant phylogenetic diversity and evolutionary history.

Spots before the eyes: revision of the saxicoline geckos of the Gehyra punctata (Squamata: Gekkonidae) species complex in the Pilbara region of Western Australia

“…Coupled with the slightly elongate body shape, large rows of spots on the dorsum and geographical isolation on the Burrup Peninsula, the combined evidence indicates this is a distinctive independently evolving lineage. Populations of Crenadactylus pilbarensis Doughty, Ellis and Oliver, 2016 from the Burrup Peninsula were also slightly genetically distinctive (Oliver et al 2010) as well as G. punctata with differences in allozymes (M. Adams and P. Doughty, unpublished data). The history of the Burrup Peninsula as a potential refugium may be of interest biogeographically, especially coupled with studies of the effects of changes in sea levels connecting current offshore islands, including Barrow Island, and the mainland.…”

“…Recently, progress has been made resolving the affinities of Gehyra to other gekkonine geckos (Heineke et al 2011;Gamble et al 2012;Sistrom et al 2014) and delimiting species boundaries (Horner 2005;Sistrom et al 2009Sistrom et al , 2013Oliver et al 2010Oliver et al , 2016Doughty et al 2012Doughty et al , 2018Hutchinson et al 2014). As pointed out 35 years ago, taxonomic progress on Gehyra has been particularly hindered by the loss of colour patterns in preservative and that 'too few specimens from too few localities have been examined ' (p. 739).…”

Systematic revision of the marbled velvet geckos (Oedura marmorata species complex, Diplodactylidae) from the Australian arid and semi-arid zones

“…Many of these lizards (but certainly not all) show a suite of morphological characters that are associated with this lifestyle-most notably dorso-ventral flattening and increased limb length (Doughty & Shine 1995;Vitt et al 1997;Goodman & Isaac 2008;Goodman et al 2008;Hoskin & Couper 2013). Saxicoline lizard 'species' also frequently comprise multiple deeply divergent evolutionary lineages-perhaps to some extent reflecting the inherently 'insular' distribution of their habitat (Oliver et al 2010;Grismer et al 2012;Werneck et al 2012;Jacobsen et al 2014). These apparent genetic and morphological correlates of specialisation suggest saxicoline lizards offer opportunities to better understand how non-adaptive (e.g.…”

“…isolation) and adaptive (e.g. habitat structure) evolutionary processes can interact to shape biodiversity (Oliver et al 2010;Grismer et al 2012;Werneck et al 2012;Jacobsen et al 2014). Their propensity to consist of divergent, morphologically cryptic and overlooked lineages also has important implications for efforts to manage and conserve evolutionary biodiversity.…”

“…Recent detailed analyses of saxicoline taxa from the arid zone have revealed deep phylogenetic divergences, and indicated that these areas have mediated the evolution and/or persistence of localized endemic lineages (Fujita et al 2010;Oliver et al 2010Oliver et al , 2014aPepper et al 2013a,b). The rocky Pilbara region in the western arid zone is a special case, with many new endemics described recently (e.g.…”