Ancient mitochondrial genomes reveal the demographic history and phylogeography of the extinct, enigmatic thylacine (Thylacinus cynocephalus)

Abstract

Aim: The Tasmanian tiger, or thylacine, is an infamous example of a recent humanmediated extinction. Confined to the island of Tasmania in historical times, thylacines were hunted to extinction <150 years after European arrival. Thylacines were also once widespread across the Australian mainland, but became extinct there c. 3,200 years before present (BP). Very little is known about thylacine biology and population history; the cause of the thylacines extirpation from the mainland is still debated and the reasons for its survival in Tasmania into the 20th century are unclear. In this study, we investigate the thylacine's phylogeography and demographic history leading up to their extinction on both the mainland and Tasmania to gain insight into this enigmatic species.Location: Southern Australia. Methods:We generated 51 new thylacine mitochondrial DNA (mtDNA) genome sequences from sub-fossil remains and historical museum specimens, and analysed them to reconstruct the species' phylogeography and demographic history. Results:We found evidence that thylacines had contracted into separate eastern and western populations prior to the Last Glacial Maximum (c. 25,000 yr BP), and that the ancient western population was larger and more genetically diverse than the historical Tasmanian population. At the time of European arrival in c. 1800 CE, Tasmanian thylacines had limited mtDNA diversity, possibly resulting from a bottleneck event broadly coincident with an El Niño-Southern Oscillation (ENSO) associated climate event, although we find some indication that the population was expanding during the late Holocene.Main Conclusions: The timing of this putative expansion, in concert with a climate event, suggests that climate change had an influence on thylacine population dynamics. Given that ENSO effects are known to have been more severe on mainland Australia, we suggest that climate change, in synergy with other drivers, is likely to have contributed to the thylacine mainland extinction.

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

“…The temporally congruent extinction of southern mainland devils and population bottleneck within the Tasmanian population 4-2k yrBP (Br€ uniche-Olsen et al, 2014) is strikingly similar to the pattern seen in thylacines(White, Mitchell, & Austin, 2018), and suggests a shared primary cause that initiated population declines. The contrasting outcomes (mainland extinction versus Tasmanian persistence) indicate that additional pressure(s) existed on the mainland population.…”

“…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.…”

“…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…”

“…(Figure 4). This could suggest that major shifts in climate likely influenced the devil populations, a common pattern for other species (Br€ uniche-Olsen, Hazlitt, & Eldridge, 2017;Kearns, Joseph, Toon, & Cook, 2014;Neaves, Zenger, Prince, & Eldridge, 2012;White, Mitchell, et al, 2018). While the island population was shielded from introduced dingoes and human intensification, the mainland population was exposed to all three impacts, suggesting a multi-causal role for the mainland extinction.…”

“…ENSO events result, critically, in greater variability in rainfall and increased intensity and duration of severe climate events, such as drought, rather than sustained aridity (Brown, 2006). During the period of increased ENSO activity both thylacines and rock wallabies declined (Br€ uniche-Olsen et al, 2017;White, Mitchell, et al, 2018). Unstable climate is associated with loss of species (Blois et al, 2010;Cooper et al, 2015), and the changes in vegetation are likely to have caused fluctuations in the abundance of herbivores, leading to reduced populations of predators (Carbone et al, 2011;Letnic & Dickman, 2006 (Petherick et al, 2013;Sandel et al, 2011).…”