Congruent phylogeographic patterns in a young radiation of live‐bearing marine snakes: Pleistocene vicariance and the conservation implications of cryptic genetic diversity

Abstract

Aim To investigate phylogeographic patterns among and within co‐occurring sea snake species from Australia's endemic viviparous Aipysurus lineage, which includes critically endangered species, and evaluate the conservation implications of geographically structured patterns of genetic divergence and diversity. Location Australia's tropical shallow water marine environments spanning four regions: Great Barrier Reef (GBR), Gulf of Carpentaria (GoC), Timor Sea (TS) and coastal WA (WAC). Methods Samples from >550 snakes representing all nine nominal Aipysurus group species were obtained from throughout their known Australian ranges. Coalescent phylogenetic analyses and Bayesian molecular dating of mitochondrial DNA, combined with Bayesian and traditional population genetic analyses of 11 microsatellite loci, were used to evaluate genetic divergence and diversity. Results Mitochondrial DNA revealed highly congruent phylogeographic breaks among co‐occurring species, largely supported by nuclear microsatellites. For each species, each region was characterized by a unique suite of haplotypes (phylogroups). Divergences between the TS, GoC and/or GBR were invariably shallow and dated as occurring 50,000–130,000 years ago, coinciding with the cyclic Pleistocene emergence of the Torres Strait land bridge. By contrast, sea snakes from coastal WA were consistently highly divergent from other regions and dated as diverging 178,000–526,000 years ago, which was not associated with any known vicariant events. Main Conclusions Previously unappreciated highly divergent sea snake lineages in coastal WA potentially represent cryptic species, highlighting this region as a high‐priority area for conservation. The cyclic emergence of the Torres Strait land bridge is consisted with observed divergences between the TS, GoC and/or GBR; however, processes involved in the earlier divergences involving the WAC remain to be determined. The observed strong population genetic structures (as surrogates for dispersal) indicate that sea snakes have limited potential to reverse population declines via replenishment from other sources over time frames relevant to conservation.

Rates of population differentiation and speciation are decoupled in sea snakes

“…The final alignment comprised 373 cytochrome b sequences of 1099 base pairs. Divergence time estimates are broadly consistent with previous studies [9,11] and most intraspecific splits are dated within the last approximately 2 Myr (figure 1). Species sampled from the two clades show contrasting phylogeographic patterns.…”

“…An important caveat of our analyses of population differentiation is that they are based on a single mitochondrial gene. However, several previous studies have shown congruent patterns of population structure based on mitochondrial and fast evolving nuclear markers in sea snakes [9,17]. This supports the utility of mitochondrial data in providing meaningful estimates of phylogeographic histories in these species.…”

Future Directions in the Research and Management of Marine Snakes

“…Quantifying the true diversity of marine snakes has been stymied by cryptic lineages and limited collection and genetic sampling. Ongoing fieldwork and integrated assessment of genetic and morphological data indicate that many widespread marine snake 'species' include multiple cryptic species, each with narrow distributions (Ukuwela et al, 2013;Sanders et al, 2014;Lukoschek, 2018a). Additionally, hybridization between closely related species with overlapping ranges may affect the true diversity of marine snakes (Sanders et al, 2014;Lukoschek, 2018b).…”

“…Population genetic structure has been studied in few of the currently recognized species of marine snake, with a bias toward the true sea snakes (e.g., Lukoschek et al, 2011;Sheehy et al, 2012; Ukuwela et al, 2014;Lukoschek, 2018a). A combination of molecular markers and spatial monitoring reveal that some species exhibit limited movement and gene flow between geographically close populations (Lukoschek and Shine, 2012).…”

“…A better understanding of connectivity and metapopulation dynamics can help define the geographic and temporal scales at which depleted populations could be replenished through migration from adjacent healthy populations. Additionally, understanding intraspecific genetic connectivity through comparative phylogeography is important for identifying hotspots of evolutionary potential (e.g., coastal Western Australia; Lukoschek, 2018a), which can assist decisions about conservation and management (e.g., determining boundaries for marine protected areas). The management of stocks requires knowledge of population structure, including effective population size and degree of connectivity among populations.…”