Speciation-by-depth on coral reefs: Sympatric divergence with gene flow or cryptic transient isolation?

The distributions of many sister species in the sea overlap geographically but are partitioned along depth gradients. The genetic changes leading to depth segregation may evolve in geographic isolation as a prerequisite to coexistence or may emerge during primary divergence leading to new species. These alternatives can now be distinguished via the power endowed by the thousands of scorable loci provided by second-generation sequence data. Here, we revisit the case of two depth-segregated, genetically isolated ecotypes of the nominal Caribbean candelabrum coral Eunicea flexuosa. Previous analyses based on a handful of markers could not distinguish between models of genetic exchange after a period of isolation (consistent with secondary contact) and divergence with gene flow (consistent with primary divergence). Analyses of the history of isolation, genetic exchange and population size based on 15,640 new SNP markers derived from RNAseq data best support models where divergence began 800K BP and include epochs of divergence with gene flow, but with an intermediate period of transient isolation. Results also supported the previous conclusion that recent exchange between the ecotypes occurs asymmetrically from the Shallow lineage to the Deep. Parallel analyses of data from two other corals with depth-segregated populations (Agaricia fragilis and Pocillopora damicornis) suggest divergence leading to depth-segregated populations may begin with a period of symmetric exchange, but that an epoch of population isolation precedes more complete isolation marked by asymmetric introgression. Thus, while divergence-with-gene flow may account for much of the differentiation that separates closely related, depth-segregated species, it remains to be seen whether any critical steps in the speciation process only occur when populations are isolated.