Genetic trade-offs and conditional neutrality contribute to local adaptation

Abstract

Divergent natural selection promotes local adaptation and can lead to reproductive isolation of populations in contrasting environments; however, the genetic basis of local adaptation remains largely unresolved in natural populations. Local adaptation might result from antagonistic pleiotropy, where alternate alleles are favoured in distinct habitats, and polymorphism is maintained by selection. Alternatively, under conditional neutrality some alleles may be favoured in one environment but neutral at other locations. Antagonistic pleiotropy maintains genetic variation across the landscape; however, there is a systematic bias against discovery of antagonistic pleiotropy because the fitness benefits of local alleles need to be significant in at least two environments. Here, we develop a generally applicable method to investigate polygenic local adaptation and identify loci that are the targets of selection. This approach evaluates allele frequency changes after selection at loci across the genome to distinguish antagonistic pleiotropy from conditional neutrality and deleterious variation. We investigate local adaptation at the qualitative trait loci (QTL) level in field experiments, in which we expose 177 F(6) recombinant inbred lines and parental lines of Boechera stricta (Brassicaceae) to their parental environments over two seasons. We demonstrate polygenic selection for native alleles in both environments, with 2.8% of the genome exhibiting antagonistic pleiotropy and 8% displaying conditional neutrality. Our study strongly supports antagonistic pleiotropy at one large-effect flowering phenology QTL (nFT): native homozygotes had significantly greater probabilities of flowering than foreign homozygotes in both parental environments. Such large-scale field studies are essential to elucidate the genetic basis of adaptation in natural populations.

Figure 1

Bivariate plot of local allele frequency changes in Colorado vs. Montana. Each data point represents a locus. Red triangles are loci displaying antagonistic pleiotropy (positive change in the local allele frequency in both environments), all of which are near the nFT QTL. Filled circles represent loci that exhibit patterns consistent with conditional neutrality (significant increase in local allele frequency in Montana, but not Colorado), and unfilled circles are neutral loci. Permutation analysis detected antagonistic pleiotropy at marker Bst027135, but local allele frequency change at this marker is only marginally significant in Colorado. In this figure, Bst027135 is coded as displaying conditional neutrality. Three loci showed negative allele frequency change in Montana, but were neutral in Colorado; those loci are represented by filled squares.

Figure 2

Change in local allele frequency across the genome from the initial experimental population to the reproductive population. These figures exclude the nFT QTL and 4 nearby loci, resulting in n= 159 markers. The change in frequency of the local allele at the nFT QTL is indicated for each experimental garden and year.

Figure 3

nFT QTL by environment interactions. Native alleles have significantly greater probability of flowering than foreign alleles in both environments. Means and standard errors were calculated based on family-level variation in the proportion of individuals that flowered. Triangles represent Montana homozygotes and circles signify Colorado homozygotes at the nFT QTL; filled symbols indicate data from RILs planted into both sites in September 2009 and monitored in 2010 (connected between sites by lines). RILs planted in fall 2008 into the Colorado garden failed to flower in 2009; experimental plants in the Montana garden from that year are indicated by unfilled, unconnected symbols.