Recent local adaptation of sockeye salmon to glacial spawning habitats

Salmonids spawn in highly diverse habitats, exhibit strong genetic population structuring, and can quickly colonize newly created habitats with few founders. Spawning traits often differ among populations, but it is largely unknown if these differences are adaptive or due to genetic drift. To test if sockeye salmon (Oncorhynchus nerka) populations are adapted to glacial, beach, and tributary spawning habitats, we examined variation in heritable phenotypic traits associated with spawning in 13 populations of wild sockeye salmon in Lake Clark, Alaska. These populations were commonly founded between 100 and 400 hundred sockeye salmon generations ago and exhibit low genetic divergence at 11 microsatellite loci (F (ST) < 0.024) that is uncorrelated with spawning habitat type. We found that mean P (ST) (phenotypic divergence among populations) exceeded neutral F (ST) for most phenotypic traits measured, indicating that phenotypic differences among populations could not be explained by genetic drift alone. Phenotypic divergence among populations was associated with spawning habitat differences, but not with neutral genetic divergence. For example, female body color was lighter and egg color was darker in glacial than non-glacial habitats. This may be due to reduced sexual selection for red spawning color in glacial habitats and an apparent trade-off in carotenoid allocation to body and egg color in females. Phenotypic plasticity is an unlikely source of phenotypic differences because Lake Clark sockeye salmon spend nearly all their lives in a common environment. Our data suggest that Lake Clark sockeye salmon populations are adapted to spawning in glacial, beach and tributary habitats and provide the first evidence of a glacial spawning ecotype in salmonids. Glacial spawning habitats are often young (i.e., < 200 years old) and ephemeral. Thus, local adaptation of sockeye salmon to glacial habitats appears to have occurred recently.