Abstract
A major goal of evolutionary biology is to understand how variation within populations gets partitioned into differences between reproductively isolated species. Here, we examine the degree to which diapause life history timing, a critical adaptation promoting population divergence, explains geographic and host-related genetic variation in ancestral hawthorn and recently derived apple-infesting races of Rhagoletis pomonella. Our strategy involved combining experiments on two different aspects of diapause (initial diapause intensity and adult eclosion time) with a geographic survey of genomic variation across four sites where apple and hawthorn flies co-occur from north to south in the Midwestern USA. The results demonstrated that the majority of the genome showing significant geographic and host-related variation can be accounted for by initial diapause intensity and eclosion time. Local genomic differences between sympatric apple and hawthorn flies were subsumed within broader geographic clines; allele frequency differences within the races across the Midwest were two to three-fold greater than those between the races in sympatry. As a result, sympatric apple and hawthorn populations displayed more limited genomic clustering compared to geographic populations within the races. The findings suggest that with reduced gene flow and increased selection on diapause equivalent to that seen between geographic sites, the host races may be recognized as different genotypic entities in sympatry, and perhaps species, a hypothesis requiring future genomic analysis of related sibling species to R. pomonella to test. Our findings concerning the way selection and geography interplay could be of broad significance for many cases of earlier stages of divergence-with-gene flow, including (1) where only modest increases in geographic isolation and the strength of selection may greatly impact genetic coupling and (2) the dynamics of how spatial and temporal standing variation is extracted by selection to generate differences between new and discrete units of biodiversity.
Highlights
A major goal of evolutionary biology is to understand how variation within interbreeding demes gets partitioned by natural selection and other evolutionary processes into differences between reproductively isolated species
In contrast to the hawthorn selection experiment [29], single nucleotide polymorphisms (SNPs) frequency differences between the seven-day and 32-day prewinter treatments in the apple fly selection experiment were significantly positively related to the differences between the earliest and latest quantiles of eclosing flies in the genome wide association study (GWAS) (r = 0.22, p < 10−2, n = 10,241; Figure 1B)
With regard to objective 1, our results show that the relationship between initial diapause intensity and eclosion time in the apple race differs from that in the hawthorn race (Figure 1)
Summary
A major goal of evolutionary biology is to understand how variation within interbreeding demes gets partitioned by natural selection and other evolutionary processes into differences between reproductively isolated species. The challenge is to discern from patterns of phenotypic and genetic differentiation, the history, factors, and processes responsible for forming and shaping clines, and how they can act, interact, and become coupled to create and maintain biodiversity [4,7,8,9,11,13,14,15,16,17,18,19,20,21,22,23] Implications from this endeavor may be strengthened by manipulation, transplant, and crossing experiments testing whether candidate phenotypes and genotypes respond as predicted to selection and cause RI [24,25,26,27]. Hybrid zones and clines provide natural and experimental laboratories to examine how new species arise and are constructed [28]
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