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Reef-building coral species are experiencing an unprecedented decline owing to increasing frequency and intensity of marine heatwaves and associated bleaching-induced mortality. Closely related species from the Acropora hyacinthus species complex differ in heat tolerance and in their association with heat-tolerant symbionts. 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 which 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 kb 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. Surprisingly, non-HE individuals with HE-like haplotypes at HES2 were more likely to bleach. At both loci, HE showed particular sequence similarity to a congener, Acropora millepora . 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. 

As climate change progresses and extreme temperature events increase in frequency, rates of disturbance may soon outpace the capacity of certain species of reef‐building coral to recover from bleaching. This may lead to dramatic shifts in community composition and ecosystem function. Understanding variation in rates of bleaching recovery among species and how that translates to resilience to recurrent bleaching is fundamental to predicting the impacts of increasing disturbances on coral reefs globally. We tracked the response of two heat sensitive species in the genusAcroporato repeated bleaching events during the austral summers of 2015 and 2017. Despite a similar bleaching response, the speciesAcropora gemmiferarecovered faster based on transcriptome‐wide gene expression patterns and had a more dynamic algal symbiont community thanAcropora hyacinthusgrowing on the same reef. Moreover,A. gemmiferahad higher survival to repeated heat extremes, with six‐fold lower mortality thanA. hyacinthus. These patterns suggest that speed of recovery from a first round of bleaching, based on multiple mechanisms, contributes strongly to sensitivity to a second round of bleaching. Furthermore, our data uncovered intragenus variation in a group of corals thought generally to be heat‐sensitive and therefore paint a more nuanced view of the future health of coral reef ecosystems against a backdrop of increasing thermal disturbances.