Ancient stickleback genomes reveal the early stages of parallel adaptation

Abstract

The parallel evolution of traits and their underlying genetic basis is well studied; however, studies of the parallel chronology of adaptive genetic changes remain scarce. The probability of parallel genetic change should be increased by the clustering of adaptive alleles in regions of suppressed recombination, particularly for genes that have large fitness or phenotypic effects. The threespine stickleback is a model system for studying parallel evolution, here we present genomic data from nine subfossil stickleback bones dated to 14.8-0.7 KYR BP in age. Comparing the four highest coverage genomes, which represent different stages along the marine-freshwater divergence continuum, we find that the accumulation of freshwater ancestry is clustered rather than randomly distributed throughout the marine-freshwater divergent regions of the genome. We consistently find freshwater ancestry on chromosome IV at the early stages of freshwater adaptation. Regions of chromosome IV contain the greatest genetic differentiation between marine and freshwater ecotypes and among the highest density of quantitative trait loci. These include Ectodysplasin (EDA), a large-effect pleiotropic locus associated with defensive armor and variation in neurosensory and behavioral traits. Freshwater ancestry in the subfossils is also consistently found at inversions and X chromosome early in the adaptive process. Our findings add to emerging evidence that freshwater adaptation in threespine stickleback could have a staggered but predictable temporal dynamic.