TY - JOUR

T1 - Ancient DNA tracks the mainland extinction and island survival of the Tasmanian devil

AU - Brüniche-Olsen, Anna

AU - Jones, Menna E.

AU - Burridge, Christopher P.

AU - Murchison, Elizabeth P.

AU - Holland, Barbara R.

AU - Austin, Jeremy J.

N1 - Funding Information: Ecological Society of Australia Incorporated; Royal Society of NSW; Australian Research Council Linkage Grant, Grant/Award Number: LP0989613; Save the Tasmanian Devil Appeal Eric Guiler; Holsworth Wildlife Research Endowment; National Climate Change Adaptation Research Facility (NCCARF); Australian Research Council Future Fellowship, Grant/Award Number: FT100100250 Funding Information: We thank Chris Turney, Chris Johnson, Barry Brook and the many reviewers and editors from multiple journal submissions for constructive feedback on the manuscript. Simon Ho provided excellent advice on obtaining substitution rate from heterochronous data. We are grateful for funding provided by the Australian Research Council Linkage Grant scheme (LP0989613), the Save the Tasmanian Devil Appeal Eric Guiler grant, the Holsworth Wildlife Research Endowment, the National Climate Change Adaptation Research Facility (NCCARF), the Ecological Society of Australia (ESA) and the Royal Zoological Society of New South Wales for an Ethel Mary Reid grant. MJ was supported by an Australian Research Council Future Fellowship (FT100100250). We thank everyone who collected Tasmanian devil samples in the field: wildlife biologists from Save the Tasmanian Devil Program and University of Tasmania students. Sarah Bray and Vicki Thompson assisted with DNA extraction and mitogenome sequencing of ancient devil samples. We thank the Western Australian Museum, Museum Victoria, the Oxford University Museum, the American Museum of Natural History, the Tasmanian Museum and Art Gallery, the Queen Victoria Museum and Art Gallery and the Australian National Wildlife Collection (CSIRO) for permission to sample museum specimens. Publisher Copyright: © 2018 John Wiley & Sons Ltd

PY - 2018

Y1 - 2018

N2 - 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 ~3,000 years 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 ~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 ~3,000 years 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 Niño 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.

AB - 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 ~3,000 years 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 ~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 ~3,000 years 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 Niño 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.

KW - ancient DNA

KW - climate change

KW - demographic history

KW - extinction

KW - genetic diversity

KW - Holocene

KW - mitochondria

KW - phylogeography

KW - Tasmanian devil

U2 - 10.1111/jbi.13214

DO - 10.1111/jbi.13214

M3 - Journal article

AN - SCOPUS:85044639131

VL - 45

SP - 963

EP - 976

JO - Journal of Biogeography

JF - Journal of Biogeography

SN - 0305-0270

IS - 5

ER -