Copy number variants at genomic loci evolve at a high rate, are linked to many different diseases, and play a role in adaptive evolution in humans and other organisms. Here we show that stickleback fish from freshwater environments have rapidly and repeatedly evolved an expanded number of copies of a gene family involved in muscle development, Myosin Heavy Chain 3 Cluster C (MYH3C), compared to marine populations. Differences in copy number between marine and freshwater fish are maintained even in the presence of gene flow, suggesting that MYH3C changes represent adaptive divergence between ecotypes. Copy number expansion occurs by tandem duplication of MYH3C coding and regulatory regions on the stickleback sex chromosome. We identify a muscle regulatory enhancer within the expanded MYH3C region and show that elevated copy number is associated with developmental and tissue-specific increases in corresponding mRNA expression levels in skeletal muscle. Common MYH3C clusters include 3-, 4-, 5-, and 6-copy variants that likely evolved through a combination of microhomology-mediated break repair and non-allelic homologous recombination. Our results provide a new example of copy number changes in a wild species and identify CNVs as potential “hotspots” of repeated adaptive evolution.

Copy number variants at genomic loci evolve at a high rate, are linked to many different diseases, and play a role in adaptive evolution in humans and other organisms. Here we show that stickleback fish from freshwater environments have rapidly and repeatedly evolved an expanded number of copies of a gene family involved in muscle development, Myosin Heavy Chain 3 Cluster C (MYH3C), compared to marine populations. Differences in copy number between marine and freshwater fish are maintained even in the presence of gene flow, suggesting that MYH3C changes represent adaptive divergence between ecotypes. Copy number expansion occurs by tandem duplication of MYH3C coding and regulatory regions on the stickleback sex chromosome. We identify a muscle regulatory enhancer within the expanded MYH3C region and show that elevated copy number is associated with developmental and tissue-specific increases in corresponding mRNA expression levels in skeletal muscle. Common MYH3C clusters include 3-, 4-, 5-, and 6-copy variants that likely evolved through a combination of microhomology-mediated break repair and non-allelic homologous recombination. Our results provide a new example of copy number changes in a wild species and identify CNVs as potential “hotspots” of repeated adaptive evolution.

With an experimental approach using mesocosms, we tested whether crayfish addition would alter the prey community structure in the environment, and whether this would change F1 hybrid fitness relative to pure Limnetic and Benthic threespine stickleback.

Incipient species often coexist in sympatry before complete reproductive isolation has evolved between them. How do they persist in the face of hybridization and gene flow? The challenge is more acute than ordinary ecological coexistence not only because gene flow erodes and recombines genetic differences, but also because selection against hybrids can destabilize population sizes. We estimated gene flow and selection against hybrid genotypes between sympatric limnetic and benthic species of threespine stickleback in two British Columbia lakes. First-generation hybrids are present at a rate of about 2%. To estimate selection, we compared the frequency distribution of ancestry proportions between juvenile and adult samples. We also used genomic simulation with assortative mating in an ecological model to determine how much selection is required to reproduce observed genotype frequencies. Results from the two approaches were comparable and yielded estimated selection coefficients S against the least fit ancestry proportion (within backcross range) between 0.5 – 0.6. Surprisingly, selection was found to be only slightly weaker than that leading readily to collapse and fusion in our simulations, suggesting that sympatric stickleback species are close to a coexistence boundary. Moderately strong selection appears to be required for coexistence with even low levels of gene flow. We suggest that larger niche differences are required to stabilize coexistence with gene flow than without gene flow. This helps to explain why successful sympatric species that hybridize often show conspicuous ecological and phenotypic differences.

AbstractMutations 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 QTL 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 observed allele frequency changes at the Eda gene in an Alaskan lake population colonized by marine stickleback in the 1980’s. The frequency of the freshwater Eda allele rose steadily over multiple generations and reached 95% within 20 years, yielding a similar estimate of selection, s = 0.49 ± 0.05. 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.

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 QTL 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 observed allele frequency changes at the Eda gene in an Alaskan lake population colonized by marine stickleback in the 1980’s. The frequency of the freshwater Eda allele rose steadily over multiple generations and reached 95% within 20 years, yielding a similar estimate of selection, s = 0.49 ± 0.05. 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.

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