A few stickleback suffice for the transport of alleles to new lakes

Abstract

Threespine stickleback populations provide a striking example of local adaptation to divergent habitats in populations that are connected by recurrent gene flow. These small fish occur in marine and freshwater habitats throughout the Northern Hemisphere, and in numerous cases the smaller freshwater populations have been established \"de novo\" from marine colonists. Independently evolved freshwater populations show similar phenotypes that have been shown to derive largely from the same standing genetic variants. Geographic isolation prevents direct migration between the freshwater populations, strongly suggesting that these shared locally adaptive alleles are transported through the marine population. However it is still largely unknown how gene flow, recombination, and selection jointly impact the standing variation that might fuel this adaptation. Here we use individual-based, spatially explicit simulations to determine the levels of gene flow that best match observed patterns of allele sharing among habitats in stickleback. We aim to better understand how gene flow and local adaptation in large metapopulations determine the speed of adaptation and re-use of standing genetic variation. In our simulations we find that repeated adaptation uses a shared set of alleles that are maintained at low frequency by migration-selection balance in oceanic populations. This process occurs over a realistic range of intermediate levels of gene flow that match previous empirical population genomic studies in stickleback. Examining these simulations more deeply reveals how lower levels of gene flow leads to slow, independent adaptation to different habitats, whereas higher levels gene flow leads to significant mutation load - but an increased probability of successful population genomic scans for locally adapted alleles. Surprisingly, we find that the genealogical origins of most freshwater adapted alleles can be traced back to the original generation of marine individuals that colonized the lakes, as opposed to subsequent migrants. These simulations provide deeper context for existing studies of stickleback evolutionary genomics, and guidance for future empirical studies in this model. More broadly, our results support existing theory of local adaptation but extend it by more completely documenting the genealogical history of adaptive alleles in a metapopulation.