Adaptive Variation Amid High Gene Flow Across a Broad Latitudinal Gradient in the Reef-Building Honeycomb Worm,...

Climate change is already altering, and will continue to reshape, the persistence and spatial structure of marine populations. Understanding metapopulation connectivity and local adaptation is therefore critical for identifying both vulnerable populations and those with adaptive resilience. We applied a seascape genomics approach to investigate connectivity patterns and adaptive responses in the honeycomb worm, Sabellaria alveolata-an intertidal ecosystem engineer that supports high biodiversity and provides essential ecological functions. A total of 286 individuals from 17 sites spanning the entire latitudinal range were genotyped to assess population structure and local adaptation. Outlier analyses (BayeScan and OutFlank) identified six adaptive and 2117 neutral SNPs. Neutral SNP analysis revealed low to moderate genetic differentiation, indicating well-connected populations. Admixture with possible ancestral gene pools in Southern Edge and Biscay populations suggests the persistence of unique genetic diversity. While connectivity is likely driven by natural larval dispersal, human-mediated transport resulting from support vessels, aquaculture, marine debris and expanding offshore and coastal infrastructure may also facilitate gene flow, shaping observed genetic patterns. Despite this high connectivity, we detected genetic signatures of adaptation to temperature, salinity and net primary productivity, with adaptive SNPs linked to genes involved in molecular and physiological responses to these environmental factors. Our findings suggest that S. alveolata is likely resilient to climate change and other anthropogenic pressures, making it a valuable model for investigating the genetic and physiological underpinnings of marine population resilience.