Reef-building coral species are experiencing an unprecedented decline due to increasing frequency and intensity of marine heatwaves and associated bleaching-induced mortality. Closely related species of reef building corals from the Acropora hyacinthus species complex differ in heat tolerance and in their association with heat-tolerant symbionts, as well as growth rate, colony morphology and skeletal density.

We used low-coverage full genome sequencing of 114 colonies monitored across the 2015 bleaching event in American Samoa to determine the genetic differences among four cryptic species (termed HA, HC, HD, and HE) that have diverged in these species traits. Cryptic species differed strongly at thousands of single nucleotide polymorphisms across the genome that are enriched for amino acid changes in the bleaching-resistant species HE. In addition, HE also showed two particularly divergent regions with strong signals of differentiation. One approximately 220-kilobase locus, HES1, contained the majority of fixed differences in HE. A second locus, HES2, was fixed in HE but polymorphic in the other cryptic species, in which HE-like genotypes were associated with increased bleaching sensitivity. At both loci, HE showed particular sequence similarity to a congener, A. millepora. This trans-species similarity could reflect introgression or deep ancestral polymorphism. Between these closely related species, differentiated loci show strong signatures of selective sweeps, introgression or long-term balancing selection, and a possible role for epistasis. Overall, resilience to bleaching during the third global bleaching event was strongly structured by host cryptic species, buoyed by differences in symbiont associations between these species.