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

Abstract

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.

Keywords: Ectodysplasin; fitness mapping; genetics of adaptation; natural selection; stickleback.

Fig. 1.

Design of the pond experiment. (A) Entrance to the Little Campbell River from the Strait of Georgia, BC. (B) Cranby Lake, BC. (C) A single intercross (F0) was made between a marine (anadromous) stickleback collected in the Little Campbell River and a freshwater-resident stickleback from Cranby Lake. Example specimens are stained with alizarin red to highlight bone. The marine population is fully plated (MM genotype at the Eda locus), whereas the freshwater population has few lateral plates (FF at Eda). First generation (F1) hybrids were crossed in the laboratory to produce second-generation (F2) hybrids that were introduced to a freshwater pond at the University of British Columbia. (D) Author M.E.A. on the experimental pond. (E) Author K.B.M. returning adult F2 hybrids to the pond after measurement.

Fig. 2.

(A) QTL map of chromosome IV for F2 female fitness measured as the number of surviving offspring. Family identity (unique combination of F1 parents) was included as a covariate. The left vertical axis indicates LOD score for fitness (black line) and body size (standard length; yellow) QTL maps. The right vertical axis indicates LOD score for lateral plates (red). (B) Genomic region surrounding the peak QTL markers for armor and fitness. A small 20-kb region contains the Eda, Tnfsf13b, and Garp genes [ENSEMBL display of gasAcu1 assembly (46)], a previously mapped regulatory SNP located in an enhancer controlling Wnt-responsive Eda expression in developing armor plates [chrIV:12811481 (47)], and the peak QTL markers for armor plate morph (chrIV:12811933) and for fitness (chrIV:12815024) in the pond experiment.

Fig. 3.

Number of surviving offspring (fitness) of individual F2 females differing in genotype at the peak marker in the QTL map for fitness (Fig. 2). MM females are homozygous for the ancestral marine allele, FF females have two copies of the derived freshwater allele, and MF females are heterozygous. Horizontal line segments are means. Vertical span of shaded region is the 95% confidence intervals for the corresponding mean, conditional on F1 × F1 family identity.

Fig. 4.

Relative frequency distribution of genotypes at the peak marker for fitness in the F3 offspring generation (filled bars) compared with that of their F2 mothers (open bars). MM individuals are homozygous for the ancestral marine allele, FF individuals have two copies of the derived freshwater allele, and MF individuals are heterozygous. Vertical lines indicate ±1 SE.

Fig. 5.

Relationship between body size (standard length) of F2 females and their numbers of surviving offspring. Regression line and 95% confidence interval for predicted values are conditional upon family identity and F2 sampling date. Points are displaced vertically by a small random amount to reduce overlap. Dashed line indicates the Poisson regression fit to the same data. A single outlier having a standard length of 2.55 cm and 0 offspring was left out of the analysis.

Fig. 6.

Allele frequency changes over time at the Eda locus after colonization of a freshwater lake by marine fish in the 1980s. (A) Loberg Lake. (B) Observed frequency change of the low-armor Eda allele (points) compared with the predicted frequency (dotted line) from the fitted model with a selection coefficient estimated as s = 0.49 ± 0.05 SE. (C) Pairwise F_st between the earliest sample in 1992 and subsequent samples to 2008. Significantly faster differentiation over time is observed at Eda (filled circles), than at three putatively neutral microsatellite loci (Stn60, Stn239, and Stn277; open symbols). The two figures use different year spans.