Broad scale agreement between intertidal habitats and adaptive traits on a basis of contrasting population genetic structure

Understanding the extent to which neutral processes and adaptive divergence shape the spatial structure of natural populations is a major goal in evolutionary biology and is especially important for the identification of significant levels of biodiversity. Our results identified replicated habitat-specific (adaptive) phenotypic divergence in the brown macroalga Fucus vesiculosus that is independent of population (neutral) genetic structure. F. vesiculosus inhabits contiguous and contrasting marine to estuarine intertidal habitats. Combining analyses of genetic and phenotypic traits of populations living under differential selective regimes (estuaries and open coast), we investigated levels of neutral genetic differentiation and adaptive physiological responses to emersion stress. In southwest England (SW UK) and northern Iberia (N. Iberia), populations living in estuaries and marine coastal habitats were genetically characterized at six microsatellite loci. In N. Iberia, two clades with limited admixture were recovered, each including one open coast site and the adjacent estuarine location. In contrast, SW UK samples clustered according to habitat and formed three distinct groups of genotypes; one including the two open coast locations and the other two representing each of the estuarine sites. Temperature loggers revealed distinct emersion regimes that characterized each habitat type independently of the region, while water and air temperature profiles showed site-specific trends. Despite acclimation under usual conditions, trait means of emersion stress resilience showed a strong phenotypic divergence between habitats, consistent with environmental clines in exposure time observed in the different habitats. We demonstrate that neutral genetic clusters do not reflect locally adapted population units. Our results identified replicated habitat-specific (adaptive) phenotypic divergence that is independent of population (neutral) genetic structure in F. vesiculosus. The significance of such findings extends beyond the theoretical evolutionary and ecological interest of discovering parallel adaptive responses to the broader implications for conservation of intraspecific biodiversity.