Ancient genomic variation underlies repeated ecological adaptation in young stickleback populations

Abstract

Adaptation in the wild often involves standing genetic variation (SGV), which allows rapid responses to selection on ecological timescales. However, we still know little about how the evolutionary histories and genomic distributions of SGV influence local adaptation in natural populations. Here, we address this knowledge gap using the threespine stickleback fish (Gasterosteus aculeatus) as a model. We extend restriction site-associated DNA sequencing (RAD-seq) to produce phased haplotypes approaching 700 base pairs (bp) in length at each of over 50,000 loci across the stickleback genome. Parallel adaptation in two geographically isolated freshwater pond populations consistently involved fixation of haplotypes that are identical-by-descent. In these same genomic regions, sequence divergence between marine and freshwater stickleback, as measured by dXY, reaches tenfold higher than background levels and genomic variation is structured into distinct marine and freshwater haplogroups. By combining this dataset with a de novo genome assembly of a related species, the ninespine stickleback (Pungitius pungitius), we find that this habitat-associated divergent variation averages six million years old, nearly twice the genome-wide average. The genomic variation that is involved in recent and rapid local adaptation in stickleback has therefore been evolving throughout the 15-million-year history since the two species lineages split. This long history of genomic divergence has maintained large genomic regions of ancient ancestry that include multiple chromosomal inversions and extensive linked variation. These discoveries of ancient genetic variation spread broadly across the genome in stickleback demonstrate how selection on ecological timescales is a result of genome evolution over geological timescales, and vice versa.