The mode of speciation during a recent radiation in open-ocean phytoplankton

Despite the enormous ecological importance of marine phytoplankton, surprisingly little is known about how new phytoplankton species originate and evolve in the open ocean, in the absence of apparent geographic barriers that typically act as isolation mechanisms in speciation. To investigate the mechanism of open-ocean speciation, we combined fossil and climatic records from the late Quaternary with genome-wide evolutionary genetic analyses of speciation in the ubiquitous and abundant pelagic coccolithophore genus Gephyrocapsa (including G. huxleyi, formerly known as Emiliania huxleyi). Based on the analysis of 43 sequenced genomes, we report that the best-fitting scenario for all speciation events analyzed included an extended period of complete isolation followed by recent (Holocene) secondary contact, supporting the role of geographic or oceanographic barriers in population divergence and speciation. Consistent with this, fossil data reveal considerable diachroneity of species first occurrence. The timing of all speciation events coincided with glacial phases of glacial-interglacial cycles, suggesting that stronger isolation between the ocean basins and increased segregation of ecological niches during glaciations are important drivers of speciation in marine phytoplankton. The similarity across multiple speciation events implies the generality of this inferred speciation scenario for marine phytoplankton.