Mutation rate estimate and population genomic analysis reveals decline of koalas prior to human arrival

The koala (Phascolarctos cinereus), an iconic Australian marsupial, has experienced substantial historical and contemporary population declines. Identifying the drivers of these declines has been hindered by limited genomic data and uncertainty regarding the koala mutation rate. Here, we report a direct estimate of the koala mutation rate, based on genome sequences of four parent-offspring trios, yielding a mean of 6.12 × 10-9 mutations per base pair per generation (95% confidence interval: 5.03 to 7.45 × 10-9). Using this estimate of the mutation rate, we reconstructed the demographic history of koalas using 457 whole-genome sequences sampled across their entire range. Our results refine the estimated timing of past changes in population size, suggesting a large decline beginning ∼100 kya, before the arrival of humans in Australia. The koala population then split into five genetic populations 6 to 30 kya, which are now distributed along the east coast of Australia. We also use our estimate of the mutation rate to infer recombination maps for each koala population, confirming lower recombination rates in marsupials than in eutherian mammals. Using these estimates of population-specific recombination rates, we inferred the timing of recent population declines for koalas across all eastern states. These findings provide critical insights into the evolutionary history of koalas, while highlighting the impacts of using species-specific estimates of evolutionary rates on the inference of demographic histories. Our estimates of the genome-wide mutation rate and population-specific recombination maps for koalas provide valuable resources for future evolutionary and conservation analyses of marsupials.