Complex Patterns of Hitchhiking Mutation Load Among Stickleback Populations

Positive selection causes beneficial alleles to rise to high frequency in a population. This can cause linked genetic variation to "hitchhike," and thereby also rise in frequency. This linked variation may include deleterious recessive alleles, previously neutrally harbored at low frequency and in heterozygous genotypes. Modeling studies have shown that local effective population size and reduced recombination rate should contribute to the probability of deleterious mutations being swept to high frequency by being linked to beneficial alleles in selective sweeps or selection on inversion karyotypes. Marine sticklebacks have repeatedly adapted to thousands of freshwater habitats that became available after the last ice age, resulting in the formation of distinct marine and freshwater ecotypes. Selection acts on ancient standing genetic variation present in marine populations, causing freshwater-adaptive alleles to increase rapidly over tens of generations. These genomic regions play a key role in the repeated freshwater adaptation of morphological, physiological, and behavioral traits, and evolve under strong selection. Thus, threespine stickleback is an ideal system for investigating the impact of hitchhiking mutation load. We estimate the mutation load in regions of low recombination, including inversions and the Eda haplotype. We find some evidence for increased accumulation of deleterious alleles in one inversion, while this is not the case for two other inversions. Inversions deviated from Hardy-Weinberg equilibrium in several populations due to an excess of homozygotes.