Rapid evolution of genetic and phenotypic divergence in Atlantic salmon following the colonisation of two new branches of a watercourse

Arne Johan Jensen, Lars Petter Hansen, Bjørn Ove Johnsen, Sten Karlsson

Selection acts strongly on individuals that colonise a habitat and have phenotypic traits that deviate from the local optima. Our objective was to investigate the evolutionary rates in Atlantic salmon (Salmo salar) in a river system (the Vefsna watershed in Norway), fewer than 15 generations after colonisation of two new branches of the watercourse for spawning, which were made available by construction of fish ladders in 1889. Differences in age and size were analysed using scale samples collected by anglers. Age and size of recaptures from a tagging experiment were compared between the three branches. Furthermore, genetic analyses of scale samples collected in the three river branches during two periods were performed to evaluate whether observed differences evolved by genetic divergence over this short period, or were the result of phenotypic plasticity. We demonstrate that evolution can be rapid when fish populations are subjected to strong selection, in spite of sympatry with their ancestral group, no physical barriers to hybridisation, and natal homing as the only reproductive isolating barrier. After fewer than 15 generations, there was evidence of genetic isolation between the two branches based on genetic variation at 96 single nucleotide polymorphism loci, and significant differences in several life history traits, including size and age at maturity. Selection against large size at maturity appears to have occurred, since large individuals were reluctant to ascend the branch with less abundant water. The estimated evolutionary rate of change in life history traits is within the upper 3 to 7% reported in other fish studies on microevolutionary rates. These findings suggest that with sufficient genetic diversity, Atlantic salmon can rapidly colonise and evolve to new accessible habitats. This has profound implications for conservation and restoration of populations and habitats in order to meet evolutionary challenges, including alterations in water regime, whether altered by climate change or anthropogenic factors.