Coral genetic structure in the Western Indian Ocean mirrors ocean circulation and thermal stress

Abstract

Global warming and rising sea temperatures are pushing many reef-building coral species towards extinction. As thermal tolerance in corals is partially heritable, identifying genes under thermal selection is critical for targeted biodiversity management. However, it remains unclear how large breaks in connectivity (>100 km of open sea) affect the spread of adaptive alleles for different coral species in discontinuous reef networks such as the West Indian Ocean (WIO). To address this, we applied a seascape genomics approach to model (i) population connectivity and (ii) thermal adaptive potentials for two keystone coral species, Acropora muricata and Pocillopora damicornis, across the WIO. For both species, corals from the Seychelles were predominantly genetically isolated from corals in Rodrigues and Mauritius, putatively an effect of regional oceanographic barriers. Furthermore, sea currents during reproductive periods better predicted genetic connectivity than did Euclidean distances for both species, highlighting that connectivity models can serve as proxies to understand dispersal potential depending on reproductive strategies. Spatial patterns of neutral genetic variation were best explained by sea surface temperature variability and mean degree heating weeks. When used in genotype- environment association (GEA) analyses, we identified hundreds of loci under putative thermal selection from linked to known heat stress responses. In A. muricata, five Sacsin genes--co- chaperones of the Hsp70 heat-shock protein involved in thermal stress response--were identified, alongside genes related to immune defence, antioxidant response, signalling, and protein folding. In contrast, only the centromere protein V, involved in mitosis, was enriched in P. damicornis. By integrating patterns of gene flow with molecular adaptations to estimate species-specific adaptive potentials, we found that large sea distances and strong oceanographic barriers inhibit the genetic exchange of adapted genotypes across the WIO, providing valuable insights to guide local and regional biodiversity management in this region.