Contemporary ancestor? Variation in marine threespine stickleback (Gasterosteus aculeatus) and its implications for adaptive divergence

Abstract

Standing genetic variation (SGV) can affect the incidence and pace of adaptation and parallel evolution. The role of SGV versus de novo mutation can be tested in ancestral-derived comparisons when the “contemporary ancestor” is extant. Assumptions about SGV in these contemporary ancestors require formal testing. The threespine stickleback is an icon of adaptive divergence, with multiple freshwater forms having evolved in parallel from a presumably panmictic, evolutionarily static marine population – in part from SGV at Ectodysplasin. Variation among marine stickleback would therefore have consequences for understanding adaptive divergence. I collected marine stickleback from eight locations between Alaska and California. Marine populations varied according to ecogeographic rules. Genotype-by-Sequencing of over 380 000 loci and 5700 SNPs revealed five genetic clusters, including one extending north from Washington to Alaska. Pairwise estimates of genetic differentiation (FST) ranged from 0.02 to 0.18. Tests of phenotypic divergence (PST-FST) for plate counts and body shape fell outside neutral evolutionary expectations, suggesting adaptive divergence may be maintaining this quantitative phenotypic variation among marine populations. Since SGV differed between populations, estimates of candidate loci exhibiting potential selection in response to freshwater colonisation varied depending on the marine population chosen as “ancestral”. It has been theorized that genome-wide heterozygosity improves fitness by buffering against asymmetry. If so, SGV could be maintained if it canalizes plate number. Although heterozygosity and asymmetry varied independently, SGV at Ectodysplasin acted as a genetic stressor that increased asymmetry. Critical thermal minima may have evolved from SGV. Contrary to expectations, marine and freshwater stickleback exhibited the same reaction norm for mitochondrial biogenesis, suggesting that biogenesis has not evolved but has retained an ancestrally adaptive phenotype. Collectively, these results reinforce that SGV is a complex and important factor in the evolution of “contemporary ancestors”, and that failure to take these complexities into account can lead to spurious interpretations of adaptation in derived populations.