Temporal variation of effective population size and gene flow determine
current patterns of genetic diversity within species, and hence the
genetic variation upon which natural selection can act. Although such
demographic processes are well understood in terrestrial organisms, they
remain largely unknown in the ocean, where species diversity is still
being described. Here, we present one of the first population genomic
studies in a cephalopod, Octopus insularis, which is distributed in
coastal and oceanic island habitats in the Atlantic Ocean, Mexican Gulf
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, suggesting that dispersal through pelagic paralarvae is
determinant for population connectivity. Together, our results show that
oceanic currents and habitat breaks are determinant in the
diversification of marine species, shaping standing genetic variability
within populations. Moreover, our results show that insular populations
are particularly vulnerable to current human exploitation and selective
pressures, calling the revision of their protection status.