Fitness maps to a large-effect locus in introduced stickleback populations

• Published in: Proceedings of the National Academy of Sciences - PNAS 2021-01, Vol.118 (3), p.1-10
• Main Authors: Schluter, Dolph, Marchinko, Kerry B., Arnegard, Matthew E., Zhang, Haili, Brady, Shannon D., Jones, Felicity C., Bell, Michael A., Kingsley, David M.
• Format: Article
• Language: English
• Subjects: Acclimatization; Adaptation, Physiological - genetics; Alleles; Animals; Biological Evolution; Biological Sciences; Ecosystem; Ectodysplasin; Evolution & development; Fitness; Fresh water; Gene frequency; Gene Frequency - genetics; Gene mapping; Genes; Genetic diversity; Genetic Fitness - genetics; Genetic variance; Genetic Variation - genetics; Genome - genetics; Genotype; Homozygotes; INAUGURAL ARTICLE; Lakes; Mutation; Mutation - genetics; Offspring; Polymorphism, Single Nucleotide - genetics; Population genetics; Populations; Quantitative trait loci; Reproductive fitness; Seawater; Smegmamorpha - genetics; Smegmamorpha - physiology; Survival
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1914889118

Mutations of small effect underlie most adaptation to new environments, but beneficial variants with large fitness effects are expected to contribute under certain conditions. Genes and genomic regions having large effects on phenotypic differences between populations are known from numerous taxa, but fitness effect sizes have rarely been estimated. We mapped fitness over a generation in an F2 intercross between a marine and a lake stickleback population introduced to a freshwater pond. A quantitative trait locus map of the number of surviving offspring per F2 female detected a single, large-effect locus near Ectodysplasin (Eda), a gene having an ancient freshwater allele causing reduced bony armor and other changes. F2 females homozygous for the freshwater allele had twice the number of surviving offspring as homozygotes for the marine allele, producing a large selection coefficient, s = 0.50 ± 0.09 SE. Correspondingly, the frequency of the freshwater allele increased from 0.50 in F2 mothers to 0.58 in surviving offspring. We compare these results to allele frequency changes at the Eda gene in an Alaskan lake population colonized by marine stickleback in the 1980s. The frequency of the freshwater Eda allele rose steadily over multiple generations and reached 95% within 20 y, yielding a similar estimate of selection, s = 0.49 ± 0.05, but a different degree of dominance. These findings are consistent with other studies suggesting strong selection on this gene (and/or linked genes) in fresh water. Selection on ancient genetic variants carried by colonizing ancestors is likely to increase the prevalence of large-effect fitness variants in adaptive evolution.