Coral Genetic Structure in the Western Indian Ocean Mirrors Ocean Circulation and Thermal Stress History

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 connectivity breaks (> 100 km of open sea) might affect the spread of adaptive alleles for different coral species in discontinuous reef networks such as the Western Indian Ocean (WIO). To address this, we applied a seascape genomics approach to model (i) population structure and (ii) thermal adaptive potentials for two keystone coral species, <i>Acropora muricata</i> and <i>Pocillopora damicornis</i>, across the WIO. Northern reefs in the Seychelles were largely genetically isolated from southern reefs in Rodrigues and Mauritius for both species, potentially driven by regional oceanographic barriers. Isolation-by-resistance calculated from ocean currents during reproductive months better explained regional genetic differences than isolation-by-distance alone. Spatial patterns of genetic variation were best captured by variables representing thermal stress, including sea surface temperature variability, accumulating heat stress, and fine-scale reef structure. Using these variables in genotype-environment association (GEA) analyses identified hundreds of loci under putative thermal selection, including several linked to genes involved in heat stress responses. We detected 12 molecular functions enriched in <i>A. muricata</i> and 20 enriched in <i>P. damicornis</i>, generally pertaining to cellular signalling, transport mechanisms, metabolism, and protein quality control, including six genes annotated as the heat-shock chaperone protein Sacsin for <i>A. muricata</i>. We produce species-specific maps estimating the putative thermally adaptive seascape across the WIO, which, when combined with population structure and previous ocean current models, indicate that the spread of heat adapted genotypes may be inhibited across the WIO. This research provides valuable insights into WIO coral population structure and thermal adaptive potentials to inform local and regional conservation management across the region.