Genetic structure and phylogeography of platypuses revealed by mitochondrial DNA

Abstract

The platypus Ornithorhynchus anatinus is an endemic monotreme species with a wide latitudinal distribution in eastern Australia, including Tasmania. Understanding of the phylogeography within this species is very limited at present and represents a gap in the documentation of Australia's unique biodiversity. We analysed mitochondrial DNA sequences (partial control region and complete cytochrome b, including portions of flanking tRNAs) of 74 individuals from across the distribution of the species. Phylogenetic analysis of the concatenated sequences corroborated the primary split within the platypus, showing two major clades: one from mainland Australia and the other from Tasmania/King Island. Estimates of divergence times suggest that these clades last shared a common mitochondrial ancestor~0.7-0.94 Ma. Using an extended dataset of partial control region sequences from 284 individuals, we found evidence of genetic structure between river basins, primarily within mainland Australia, as well as an additional divergent lineage in North-eastern Australia. Overall, few haplotypes were shared between river basins. Analyses of molecular variance of the control region sequences indicated low rates of gene flow and significant divergence, particularly at the river basin and geographical area scales.

Ancient DNA tracks the mainland extinction and island survival of the Tasmanian devil

“…The Tasmanian and southern mainland populations of devils show a clear pre‐LGM phylogenetic split, suggesting a lack of gene flow across the Bass Strait land bridge during the LGM. This pattern is consistent with several other mammals, frogs and reptiles, which show pre‐LGM divergence and no evidence for subsequent dispersal (Dubey & Shine, ; Frankham, Handasyde, & Eldridge, ; Gongora et al., ; Symula, Keogh, & Cannatella, ). In contrast, the thylacine (White, Mitchell, et al, ) and several other reptiles and frogs (Chapple, Keogh, & Hutchinson, ; Schäuble & Moritz, ) show evidence of dispersal and gene flow across the Bass Strait land bridge in the late Pleistocene.…”

“…Typically these patterns are consistent with two wellcharacterized biogeographic barriers-the Nullarbor and Lake Eyre regions-at Plio-Pleistocene timescales. In contrast, devils along with several species of birds and mammals (Clegg, Hale, & Moritz, 1998;Cooper, Adams, & Labrinidis, 2000;Dolman & Joseph, 2015;Pestell, Cooper, Saint, & Petit, 2007) show pre-LGM divergence and no evidence for subsequent dispersal (Dubey & Shine, 2010;Frankham, Handasyde, & Eldridge, 2016;Gongora et al, 2012;Symula, Keogh, & Cannatella, 2008). In contrast, the thylacine (White, Mitchell, et al, 2018) and several other reptiles and frogs (Chapple, Keogh, & Hutchinson, 2005…”

Did postglacial sea-level changes initiate the evolutionary divergence of a Tasmanian endemic raptor from its mainland relative?

“…Whereas changes in climate across the LGM have been implicated for extirpation and recolonization of mid-latitude populations in the Northern Hemisphere [72], they appear to have been less influential on species distributions at similar latitudes in the Southern Hemisphere [73,74]. Other animals presently distributed in Tasmania and mainland Australia, including prey species of A. audax, exhibit genetic divergences compatible with occupation of Tasmania during glacial periods [24,[75][76][77]. Therefore, the hypothesis that we have reconstructed the first arrival in Tasmania of A. audax can only be rejected by fossil or subfossil evidence for an earlier occupation, of which we are unaware.…”

“…240 km) but shallow (less than 70 m; figure 2; [23]) seaway (Bass Strait), with high tectonic stability, such that repeated terrestrial connections existed during the Pleistocene, most recently during the LGM [10]. Tasmanian and mainland populations of several species have also undergone trait divergence with respect to morphology, physical appearance, behaviour and life-history characters [24][25][26]. In particular, a high proportion of the Tasmanian terrestrial avifauna (20 out of 145 species) exhibit divergence from mainland relatives at a level considered worthy of subspecies recognition [27].…”

Influence of drainage divides versus arid corridors on genetic structure and demography of a widespread freshwater turtle, Emydura macquarii krefftii, from Australia

“…The "Burdekin Gap" arid corridor is a well-recognized vicariant barrier driving north-south divergence in many terrestrial animal lineages (Chapple et al 2011), and its influence dates to the mid-to-late-Miocene or Pliocene (James and Moritz 2000;Moussalli et al 2005). More recently, molecular studies of several wide-ranging freshwater taxa also report deep north-south lineage disjunction congruent with the Gap (e.g., freshwater fishes, Wong et al 2004;Jerry 2008;Unmack and Dowling 2010; and platypus, a freshwater mammal, Gongora et al 2012). However, the Burdekin drainage hosts substantially lower species diversity of freshwater fishes compared with adjacent drainages, and inadequate sampling has so far precluded accurate assessment of possible alternative historical barriers to freshwater dispersal.…”