Long-distance gene flow and contrasting population structures of reef-building corals and their algal symbionts inform adaptive potential across the Western Pacific

The genetic diversity and connectivity of reef-building coral populations are key to their survival in warming oceans. Yet our understanding of corals demographic resilience and adaptive potential is complicated by cryptic species diversity, wide geographic distributions, and complex coral-algal symbioses. To address these challenges, we investigated genetic connectivity and diversity of the broadcast-spawning coral Acropora spathulata and its associated Symbiodiniaceae across 29 reefs spanning the Great Barrier Reef, the Coral Sea, and New Caledonia, using whole-genome sequencing of 1,088 colonies. We identified four genetically distinct coral populations that diverged between 0.27 and 0.65 million years ago, likely due to geographic isolation across thousands of kilometers. These populations maintained asymmetrical gene flow along major ocean currents despite demographic isolation, and sustained large local effective population sizes ([~]2,900), supported by a high dispersal range of [~]100 km per generation. In contrast, their Symbiodiniaceae partners varied over finer spatial scales, with five distinct Cladocopium taxa distributed along latitudinal and cross-shore gradients, likely driven by local environmental conditions. These results suggest that high dispersal capacity and large local population size promote demographic resilience within reef systems, while environment-specific symbioses and long-distance gene flow across reef-systems support adaptation and evolutionary rescue.