Illuminating Deep Reef Refugia: Horizontal and Vertical Genomic Connectivity of Seriatopora hystrix in the Ryukyu...

Shallow coral reefs are under threat from anthropogenic stress and climate change. Mesophotic coral ecosystems (MCEs), found in deeper, cooler and less impacted waters, are proposed as potential refugia or larval sources for shallow reefs. However, this hypothesis of such deep-reef refugia is now controversial because their effectiveness is not uniform across regions and depths. Here, we investigated whether MCEs in the Ryukyu Islands act as refugia or support shallow reef recovery. Using genome-wide SNP data from 389 Seriatopora hystrix individuals collected across depths of 1-51 m, we first identified at least three cryptic lineages (α, β and γ) that were not strictly associated with depth or region. Following lineage assignment, results from MLPE and Bayesian clustering indicated that the magnitude of genetic structure differed among lineages but consistently increased with spatial separation, both among sites and across depth gradients. Notably, the genetic structure associated with 30 m depth difference was equivalent to that observed across 16-32 km of horizontal distance. Assignment tests revealed lineage-specific connectivity, from weak between sites to relatively strong across depths and nearby sites. Demographic analyses further showed a decline in population size in the deep population of the γ lineage, in which no intermediate population was identified. Aside from lineage-specific differences, connectivity across different depth habitats appears to depend on the continuity of habitats. Therefore, conservation strategies that include mesophotic reef habitats under future climate change should consider both cryptic genetic lineages and topographic continuity of habitats spanning different depths.