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 by uncertainty regarding the koala mutation rate. Here, we provide the first direct estimate of the koala mutation rate, based on four parent-offspring trios, yielding a mean of 6.12×10 ^-9 mutations per base pair per generation (95% confidence interval: 5.03—7.45×10 ^-9 ). Using this estimate of the rate, we reconstructed the demographic history of koalas using 458 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 modern humans in Australia. The koala population then split into five genetic populations 6—30 kya, which are now spread across >3500 km on the east coast of Australia. We also use the koala mutation rate to infer recombination maps for each population, confirming lower recombination rates in marsupials than in eutherian mammals. These findings provide critical insights into the evolutionary history of koalas, while highlighting the impact of using species-specific evolutionary rates in the inference of demographic histories and recombination landscapes. 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.