Ancient stickleback genomes reveal the chronology of parallel adaptation

Abstract

Parallel evolution of traits and their underlying genetic basis is well-studied, however, studies of parallel chronology of adaptive genetic changes remain scarce. Threespine stickleback are a model system for studying parallel evolution. 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 continuum, we find that freshwater ancestry is often 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 EDA, a large-effect pleiotropic locus associated with defensive armour and variation in neurosensory and behavioural traits. Freshwater ancestry is also found at inversions in the subfossils early in the adaptive process. Our findings add to the growing body of evidence that freshwater adaptation in threespine stickleback has a staggered but predictable temporal dynamic. 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 a large phenotypic effect.