Coastal marine ecosystems are highly productive and important for global fisheries. To mitigate over-exploitation and to establish efficient conservation management plans for species of economic interest, it is necessary to identify the oceanographic barriers that condition divergence and gene flow between populations with those species, and that determine their relative amounts of genetic variability. Here, we present the first population genomic study of an Octopus species, Octopus insularis, which was described in 2008 and is distributed in coastal and oceanic island habitats in the tropical Atlantic Ocean, Gulf of Mexico and the Caribbean Sea. Using genomic data, we identify the South Equatorial current as the main barrier to gene flow between southern and northern parts of the range, followed by discontinuities in the habitat associated with depth. We find that genetic diversity of insular populations significantly decreases after colonization from the continental shelf, also reflecting low habitat availability. Using demographic modelling, we find signatures of a stronger population expansion for coastal relative to insular populations, consistent with estimated increases in habitat availability since the Last Glacial Maximum. The direction of gene flow is coincident with unidirectional currents and bidirectional eddies between otherwise isolated populations. Together, our results show that oceanic currents and habitat breaks are determinant in the diversification of coastal marine species where adults have a sedentary behavior but paralarvae are dispersed passively, shaping standing genetic variability within populations. Lower genetic diversity within insular populations implies that these are particularly vulnerable to current human exploitation and selective pressures, calling for the revision of their protection status.

single-end ddRAD-seq data demultiplexed with ipyrad v.0.9.50