Experimental evidence of genome-wide impact of ecological selection during early stages of speciation-with-gene-flow

Abstract

Theory predicts that speciation-with-gene-flow is more likely when the consequences of selection for population divergence transitions from mainly direct effects of selection acting on individual genes to a collective property of all selected genes in the genome. Thus, understanding the direct impacts of ecologically based selection, as well as the indirect effects due to correlations among loci, is critical to understanding speciation. Here, we measure the genome-wide impacts of host-associated selection between hawthorn and apple host races of Rhagoletis pomonella (Diptera: Tephritidae), a model for contemporary speciation-with-gene-flow. Allele frequency shifts of 32 455 SNPs induced in a selection experiment based on host phenology were genome wide and highly concordant with genetic divergence between co-occurring apple and hawthorn flies in nature. This striking genome-wide similarity between experimental and natural populations of R. pomonella underscores the importance of ecological selection at early stages of divergence and calls for further integration of studies of eco-evolutionary dynamics and genome divergence.

Keywords: Adaptation; Rhagoletis pomonella; experimental genomics; genomics of speciation; speciation-with-gene-flow.

Figure 1

Relationship of diapause life history difference between the R. pomonella host races and divergent ecological rearing conditions imposed in the selection experiment. (a) Fruit on apple trees ripens 3–4 weeks earlier than hawthorn fruit (dashed lines). Apple flies eclose earlier as adults (solid lines) and are exposed to warmer temperatures as pupae in the soil for a longer period of time before winter than hawthorn flies (shaded brackets); (b) In the selection experiment, hawthorn flies were exposed to a short (7‐day) vs. long (32‐day) pre‐winter period to emulate the time difference experienced by hawthorn vs. apple‐fly pupae in nature.

Figure 2

Evidence for genome‐wide effects of selection on divergence between the host races. Genome‐wide sliding window comparison of allele frequency shifts in the selection experiment (red line; left axis) vs. divergence between field‐collected sympatric host races (blue line; right axis) along chromosomes 1–5 (see Methods for details concerning calculation of values). Circles above panels denote SNPs showing statistically significant response in the selection experiment (open red) or difference between the host races (solid blue). Correlation coefficient (r) is reported independently for each chromosome illustrating the association between allele frequency shifts in the selection experiment and allele frequency differences between sympatric host races in nature (all P < 10⁻⁴). Note, lines represent sliding window averages taken across the genome in 2 centi‐Morgan intervals around each SNP, not the raw allele frequency differences.

Figure 3

Polygenic response to selection for (a) all 32 455 SNPs and for (b) the 154 SNPs showing significant difference in the selection experiment and in sympatry. Upper panels are the distributions of polygenic genotype scores (i.e. the mean proportion of hawthorn race alleles that an individual's genome possesses) for the ‘selected’ hawthorn host race (dashed red line) compared to the sympatric hawthorn (red) and apple (green) host races. The distribution of the ‘selected’ haw race reflects the degree that lengthening the pre‐winter period genomically shifted the hawthorn towards the apple race. Also shown are box plots illustrating the distribution of genotype scores.