The platypus is an egg-laying mammal which, alongside the echidna, occupies a unique place in the phylogenetic tree. Despite widespread interest in its unusual biology, little is known about its population structure or recent evolutionary history. To provide new insights into the dispersal and demographic history of this non-model species, we sequenced the genomes of 57 platypuses from across the whole species range in eastern mainland Australia and Tasmania. Using a highly-improved reference genome, we called over 6.7M SNPs, providing an informative genetic data set for population analyses. Our results show very strong population structure in the platypus, with our sampling locations corresponding to discrete populations between which there is no evidence for recent gene flow. Genome-wide data allowed us to establish that 28 of the 57 sampled individuals had at least a third-degree relative amongst other samples from the same river, often taken at different times. Taking advantage of a sampled family quartet, we estimated the de novo mutation rate in the platypus at 7.0x10-9/bp/generation, one of the first direct estimates made in a non-model organism. We estimated effective population sizes of ancestral populations and haplotype sharing between current populations, and found evidence for bottlenecks in multiple populations, and early divergence between different populations. This study demonstrates the power of whole-genome sequencing for studying natural populations of an evolutionarily important species.
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