Discovery of genetically distinct, sympatric coral lineages with temporal but not gametic reproductive isolation

Abstract

Coral species abundance and biodiversity estimates are typically based on colony macromorphology. However, such measurements often underestimate the true diversity within coral communities because morphology does not necessarily reflect behavioral or genetic divergence. We previously reported on the unusual spawning behavior of the southern Caribbean population of the brain coral Diploria labyrinthiformis (Linnaeus, 1758), which spawns in both spring and autumn. Here, using data collected from 2013 to 2021, we show that the D. labyrinthiformis population in Curaçao is comprised of two behaviorally- and genetically distinct lineages, with 93% of colonies spawning exclusively in one season or the other. The two lineages could not be distinguished based on macromorphological differences or depth but represented clearly distinct genetic clusters (FST = 0.098) based on genome-wide sequencing. We tested for prezygotic and postzygotic gametic barriers between these two lineages by fertilizing eggs released in spring 2019 with sperm collected and cryopreserved in autumn 2018. Fertilization was successful and the resulting larvae developed normally, thus eliminating gametic incompatibility or early life postzygotic barriers as explanations for the divergence between these groups. Using observations from 19 other Caribbean localities, we confirmed the co-occurrence of discrete spring- and autumn-spawning populations in several locations across a range of latitudes. Thus, we show that seasonal, temporal reproductive isolation (allochrony), but not gametic reproductive isolation, is a strong barrier to gene flow in sympatric lineages of this critically endangered reef-building coral. More broadly, our findings underscore the role of allochrony as a mechanism capable of driving genetic divergence among cryptic, sympatric coral species.