Discovery of Genetically Distinct, Sympatric Coral Lineages With Temporal but Not Gametic Reproductive Isolation

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 brain coral Diploria labyrinthiformis (Linnaeus, 1758) in Curaçao, Southern Caribbean, where this species spawns in both spring and autumn. Here, using data collected from 2013 to 2021, we show that in Curaçao, D. labyrinthiformis comprises 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 obvious macromorphological differences or depth but represented clearly distinct genetic clusters (F_ST = 0.098) based on genome-wide sequencing. We tested for prezygotic and postzygotic gametic barriers between them by fertilising eggs released in spring 2019 with sperm collected and cryopreserved in autumn 2018. Fertilisation in this unidirectional cross was successful and the resulting larvae developed normally, thus eliminating complete gametic incompatibility or early life postzygotic barriers as explanations for their divergence. Using observations from 19 other localities across the Wider Caribbean Region, we confirmed the co-occurrence of discrete spring- and autumn-spawning populations 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 in the creation and maintenance of cryptic coral lineages and the urgency of identifying, quantifying, and conserving this diversity before it is lost.