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

Aim: The Tasmanian devil (Sarcophilus harrisii), currently restricted to the island of Tasmania, was found over most of the Australian mainland prior to its extinction similar to 3,000years ago. Recent debate has focused on the roles of humans, climate change and dingoes as drivers of the mainland extinction. Determining past genetic diversity and population dynamics of both populations is a fundamental component to understand why the species went extinct on mainland Australia, but survived in Tasmania. Here, we investigate the phylogeography and demographic history of the Tasmanian devil across southern Australia over the last similar to 30k years. Location: Australia. Taxon: Tasmanian devil (Sarcophilus harrisii). Methods: We used complete and partial mitochondrial DNA (mtDNA) genomes from 202 devils representing the extinct mainland (n = 17) and the extant Tasmanian (n = 185) populations to investigate the population dynamics of southern mainland and Tasmanian devils. The samples were sub-fossil bones, historical museum specimens and modern tissue samples, dating from the present to 17k years before present. Using summary statistics, frequentist inference and Bayesian phylogenetic analysis we explored whether levels of genetic diversity were similar, and if the southern mainland experienced a gradual rather than an abrupt decline prior to its extinction. Results: MtDNA genomes from mainland devils suggest that this population was larger and had more genetic diversity than the Tasmanian population. Directly dated samples indicates that the southern mainland population expanded after the last glacial maximum and remained stable until its extinction. The Tasmanian population has much lower diversity and descends from a single mtDNA lineage similar to 3,000years ago. The recent origin for all Tasmanian mtDNA diversity is concordant with a previously documented late-Holocene population bottleneck and is broadly contemporaneous with the extinction of the southern mainland population. Main conclusions: This pattern shows striking similarity to the demographic history of thylacines, suggesting that a shared factor initiated population declines in both species on the southern mainland and in Tasmania. El Nino Southern Oscillation (ENSO)-related climate change is the only factor common to both mainland Australia and Tasmania. Additional, direct or indirect, pressures from humans and/or dingoes on the mainland may have ultimately resulted in their extinction.