Sweeping genomic remodeling through repeated selection of alternatively adapted haplotypes occurs in the first decades after marine stickleback colonize new freshwater ponds

Abstract

Heterogeneous genetic divergence can accumulate across the genome when populations adapt to different habitats while still exchanging alleles. How long does diversification take and how much of the genome is affected? When divergence occurs in parallel from standing genetic variation, how often are the same haplotypes used? We explore these questions using RAD-seq genotyping data, and show that broad-scale genomic re-patterning, fueled by standing variation, can emerge in just dozens of generations in replicate natural populations of threespine stickleback fish (Gasterosteus aculeatus). After the catastrophic 1964 Alaskan earthquake, marine stickleback colonized newly created ponds on seismically uplifted islands. We find that freshwater fish in these young ponds differ from their marine ancestors across the same genomic segments previously shown to have diverged in much older lake populations. Outside of these core divergent regions the genome shows no population structure across the ocean-freshwater divide, consistent with strong local selection acting in alternative environments on stickleback populations still connected by significant gene flow.Reinforcing this inference, a majority of divergent haplotypes that are at high frequency in ponds are shared across independent freshwater populations and are detectable, at low frequency, in the sea even across great geographic distances. Building upon previous work in this model species for population genomics, our data suggest that a long history of divergent selection and gene flow across stickleback in oceanic and freshwater habitats has created balanced polymorphism in large genomic blocks of alternatively adapted DNA sequences, ultimately stoking - and potentially channeling - rapid, parallel evolution.