Speciation across depth gradients in reef corals

Ecological speciation through adaptation to different habitats can readily occur without strong geographic isolation when the same traits underlie both ecological divergence and reproductive isolation. In light-dependent corals with environment-mediated spawning, adaptation to varying light regimes across depths provides opportunities for such speciation. We show that depth-related distributions are common among sister lineages of corals within the photic zone. We then investigated molecular drivers of depth-associated adaptive divergence by analyzing sequence variation in proteins related to environmental sensing in depth-segregated and light-dependent lineages in the Orbicella species complex. Specifically, we analyzed 1) two genetically divergent ecotypes of Orbicella faveolata across a depth gradient, and 2) two depth-segregated sister species, O. annularis and O. franksi, with different spawning times following sunset. Genome-wide analyses indicate divergence across depths occurred through adaptation via positive selection on G-protein-coupled receptors (GPCRs). These molecules mediate chemo/photo/thermo-reception, enhancing physiological adaptation across environments, and are also involved in reproductive isolation via differences in spawning time. Our study proposes a molecular mechanism for the origin of depth-segregated coral species, common across anthozoans, in which ecological divergence operates at spatial scales smaller than their larval dispersal potential, and highlights avenues contributing to generating biodiversity in the sea.