As global warming continues, reef-building corals could avoid local population declines through "genetic rescue" involving exchange of heat-tolerant genotypes across latitudes, but only if latitudinal variation in thermal tolerance is heritable. Here, we show an up-to-10-fold increase in odds of survival of coral larvae under heat stress when their parents come from a warmer lower-latitude location. Elevated thermal tolerance was associated with heritable differences in expression of oxidative, extracellular, transport, and mitochondrial functions that indicated a lack of prior stress. Moreover, two genomic regions strongly responded to selection for thermal tolerance in interlatitudinal crosses. These results demonstrate that variation in coral thermal tolerance across latitudes has a strong genetic basis and could serve as raw material for natural selection.
Can genetic adaptation in reef-building corals keep pace with the current rate of sea surface warming? Here we combine population genomics, biophysical modeling, and evolutionary simulations to predict future adaptation of the common coral Acropora millepora on the Great Barrier Reef (GBR). Genomics-derived migration rates were high (0.1–1% of immigrants per generation across half the latitudinal range of the GBR) and closely matched the biophysical model of larval dispersal. Both genetic and biophysical models indicated the prevalence of southward migration along the GBR that would facilitate the spread of heat-tolerant alleles to higher latitudes as the climate warms. We developed an individual-based metapopulation model of polygenic adaptation and parameterized it with population sizes and migration rates derived from the genomic analysis. We find that high migration rates do not disrupt local thermal adaptation, and that the resulting standing genetic variation should be sufficient to fuel rapid region-wide adaptation of A. millepora populations to gradual warming over the next 20–50 coral generations (100–250 years). Further adaptation based on novel mutations might also be possible, but this depends on the currently unknown genetic parameters underlying coral thermal tolerance and the rate of warming realized. Despite this capacity for adaptation, our model predicts that coral populations would become increasingly sensitive to random thermal fluctuations such as ENSO cycles or heat waves, which corresponds well with the recent increase in frequency of catastrophic coral bleaching events.
Although reef-building corals are declining worldwide, responses to bleaching vary within and across species and are partly heritable. Toward predicting bleaching response from genomic data, we generated a chromosome-scale genome assembly for the coral Acropora millepora. We obtained whole-genome sequences for 237 phenotyped samples collected at 12 reefs along the Great Barrier Reef, among which we inferred little population structure. Scanning the genome for evidence of local adaptation, we detected signatures of long-term balancing selection in the heat-shock co-chaperone sacsin. We conducted a genome-wide association study of visual bleaching score for 213 samples, incorporating the polygenic score derived from it into a predictive model for bleaching in the wild. These results set the stage for genomics-based approaches in conservation strategies.
Gene body methylation (GBM) has been hypothesized to modulate responses to environmental change, including transgenerational plasticity, but the evidence thus far has been lacking. Here we show that coral fragments reciprocally transplanted between two distant reefs respond predominantly by increase or decrease in genome-wide GBM disparity: The range of methylation levels between lowly and highly methylated genes becomes either wider or narrower. Remarkably, at a broad functional level this simple adjustment correlated very well with gene expression change, reflecting a shifting balance between expressions of environmentally responsive and housekeeping genes. In our experiment, corals in a lower-quality habitat up-regulated genes involved in environmental responses, while corals in a higher-quality habitat invested more in housekeeping genes. Transplanted fragments showing closer GBM match to local corals attained higher fitness characteristics, which supports GBM’s role in acclimatization. Fixed differences in GBM between populations did not align with plastic GBM changes and were mostly observed in genes with elevated FST, which suggests that they arose predominantly through genetic divergence. However, we cannot completely rule out transgenerational inheritance of acquired GBM states.
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