Comparative genomics of two closely related coral species with different spawning seasons reveals genomic regions possibly associated with gametogenesis

Marine invertebrates release their gametes at an optimal time to produce the next generation. In reef-building scleractinian corals, synchronous spawning is essential for reproductive success. Molecular mechanisms of scleractinian gametogenesis have been studied; however, the mechanism by which coral gametes mature at specific times has yet to be discovered. The present study focused on two Acropora species with different spawning seasons. In Okinawa, Japan, Acropora digitifera spawns from May to June, whereas Acropora sp. 1 spawns in August. Comparative genomic analyses revealed that 39 candidate genes are differentiated between the two species, suggesting a possible association with timing of gametogenesis. Among candidate genes, we identified an Acropora sp. 1-specific amino acid change in gene WDR59, one of the components of a mTORC1 activator, GATOR2. Since regulation of gametogenesis by mTORC1 is widely conserved among eukaryotes, the difference in timing of gamete maturation observed in the two Acropora species may be caused by a substitution in WDR59 that slightly affects timing of mTORC1 activation via GATOR2. In addition, this substitution may lead to reproductive isolation between the two species, due to different spawning periods. Thus, we propose that A. digitifera and Acropora sp. 1 species pair is an effective model for studying coral speciation and understanding the molecular mechanisms that control coral spawning timing. Significance statement (required)For successful coral reproduction, conspecific corals must spawn synchronously. Gamete production initiates coral spawning. Regulation of gamete maturation by a protein complex, mTORC1, is widely conserved among organisms, but little is known about it in cnidarians. In this study, we analyzed genomes of two closely related Acropora species with different spawning months, May/June and August. Our analyses revealed that 39 genes are genetically differentiated between the two species. One of these is a component of mTORC1 activator, suggesting that this gene may be associated with the difference in spawning times of these two species.