Local adaptation, dispersal, and gene flow in a metapopulation of sockeye salmon

Abstract

Gene flow within a metapopulation depends on the reproductive success of dispersers after immigration, but few empirical studies have measured the reproductive contributions of dispersers from distinct natal populations. The local adaptation frequently observed within metapopulations of anadromous salmonids could exert strong selection against immigrants with phenotypes adapted to ecologically distinct habitats. Here, we used genetic parentage analysis to directly measure the reproductive success of dispersers from multiple natal habitats relative to philopatric individuals within a group of geographically proximate but ecologically and genetically distinct subpopulations of stream- and beach-spawning sockeye salmon (Oncorhynchus nerka). Our results indicate that dispersers between stream-spawning populations and philopatric individuals experienced similar reproductive success, while immigrants from the beach habitat to the streams produced fewer returning adult offspring than either philopatric individuals or stream-to-stream dispersers. The difference in reproductive contribution between beach-to-stream dispersers and the other two dispersal categories was estimated to be one returning adult offspring per individual. Thus, the difference in reproductive success of dispersers between habitat types represents a strong barrier to gene flow between these sockeye salmon ecotypes. Experimental and observational studies of the homing and spawning behavior of hatchery-raised salmon have indicated that their search for high-quality spawning habitat can overcome their homing tendency. Nevertheless, the extent to which dispersal between populations is motivated by habitat selection versus navigational errors during the homing process is not well understood, especially in wild populations. Here we examined whether dispersing individuals exhibited more exploratory behavior than philopatric individuals within a metapopulation of wild sockeye salmon, which would suggest that dispersal may be influenced by comparisons between potential spawning areas. We tracked the daily locations of all adult salmon spawning in two proximate streams and determined the dispersal status for each individual by comparing its chosen spawning stream with that of its parents (as determined by genetic parentage reconstruction). Dispersers were often observed in their natal stream (8-11% of individuals) or at its mouth (29-58% of individuals) before spawning in the other stream, whereas philopatric individuals were rarely observed in their non-natal stream (0-2% of individuals) or at its mouth (1-7% of individuals). These results suggest either that the mechanism of dispersal encourages exploration or that individuals that explore are more likely to disperse. In either case, dispersers are exposed to multiple spawning habitats, potentially allowing annual variation in local environmental or demographic conditions to influence the patterns of gene flow within a metapopulation.