Diversity and divergence of two sympatric, sibling octopus species

Coleoid cephalopods have convergently evolved many traits shared with vertebrates, including camera-type eyes, large brain-to-body size ratios, and complex behaviors. Most evolutionary studies of cephalopods have compared individual genomes of taxa that diverged tens to hundreds of millions of years ago, yet very few have examined more recent evolution from a population genetics perspective. Here we present a comparative population genomic analysis of the sympatric sister species Octopus bimaculatus and Octopus bimaculoides using whole-genome resequencing. Despite similar morphologies, these species differ substantially in their life histories, ecologies, and geographic distributions. Using demographic inference, we estimated that the two species diverged on the order of one million years ago, with point estimates from independent methods spanning roughly 0.4 to 1.3 million years, and that O. bimaculatus has maintained a consistently larger effective population size since divergence. Consistent with these demographic histories, we found stronger signatures of positive selection in O. bimaculatus, including a positive correlation between recombination rate and nucleotide diversity, more selective sweeps, and a higher proportion of mutations fixed by adaptation-all consistent with more efficient natural selection in larger populations. Protein-coding genes overlapping with selective sweeps were enriched for various functions that included many related to brain and eye development, suggesting that traits characteristic of coleoid cephalopods continue to be shaped by positive selection on recent timescales in these species. Comparing coding-sequence divergence on the Z chromosome to the autosomes, we also find evidence for a female-biased mutation rate, consistent with an independent estimate from a deeper-timescale cephalopod comparison.