Extensive population decline in the Tasmanian devil predates European settlement and devil facial tumour disease

Abstract

The Tasmanian devil (Sarcophilus harrisii) was widespread in Australia during the Late Pleistocene but is now endemic to the island of Tasmania. Low genetic diversity combined with the spread of devil facial tumour disease have raised concerns for the species' long-term survival. Here, we investigate the origin of low genetic diversity by inferring the species' demographic history using temporal sampling with summary statistics, full-likelihood and approximate Bayesian computation methods. Our results show extensive population declines across Tasmania correlating with environmental changes around the last glacial maximum and following unstable climate related to increased 'El Niño-Southern Oscillation' activity.

Keywords: Bayesian likelihood; Tasmanian devil; approximate Bayesian computation; demographic history; microsatellite.

Figure 1.

(a) Map showing the nine sampling localities in Tasmania. Black dashed line indicates the approximate DFTD front in 2004 with disease-affected sites east of the front. (b) Population structure among the Tasmanian devil populations inferred from Bayesian clustering. Each bar represents the proportion of ancestry in each of the two (k = 2) clusters. Geographical regions are given above and the sampling locations below. Only samples from 2004 to 2005 are shown. (c) Most likely model of demographic history for Tasmanian devil populations tested in DIYABC (electronic supplementary material, SI 8). Abbreviations correspond to: times of divergence (T_WNE and T_NE), admixture (T_C), times of population size change (T_N and T_E) and effective population sizes (N_N, N_C, N_E, N_W, N_Na and N_Ea). The arrows correspond to admixture rates (r_N and r_E). The figure is not drawn to scale.

Figure 2.

(a) Posterior density distributions of effective population size change parameter log₁₀(r) from MSVAR v. 0.4.1b. The magnitude of change in population size (r = N₀/N₁) is estimated based on the ratio of the effective number of chromosomes in the current (N₀) and the ancestral (N₁) populations. Three independent Markov chain Monte Carlo runs were performed under a model of exponential change (solid lines) and linear change (dashed lines), respectively. The dotted horizontal line represents the prior. Log₁₀(r) < 0 corresponds to a population decline and log₁₀(r) > 0 a population expansion. Whichever demographic model was used, we did not find support for positive values (increase in population size) or for values close to zero (stable population size). (b) Posterior density distributions of current (log₁₀(N₀)) and ancestral (log₁₀(N₁)) effective population sizes from MSVAR v. 1.3 under the exponential model. Black solid lines represent log₁₀ estimates of current population size (N₀) and grey solid lines ancestral (N₁) population size. The dotted lines represent the prior distributions. All posterior distributions show a decline in population size (N₀ < N₁) over time.