Genomically correlated trait combinations and antagonistic selection contributing to counterintuitive genetic patterns of adaptive diapause divergence in Rhagoletis flies

Genomically correlated trait combinations and antagonistic selection contributing to counterintuitive genetic patterns of adaptive diapause divergence in Rhagoletis flies
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DOI:
10.1111/jeb.13952
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发表时间:
2021-11-18
影响因子:
2.1
通讯作者:
Ragland,Gregory J.
Ragland,Gregory J.
中科院分区:
生物学3区
文献类型:
--
作者:
Calvert,McCall B.;Doellman,Meredith M.;Ragland,Gregory J.

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Adaptation to novel environments can result in unanticipated genomic responses to selection. Here, we illustrate how multifarious, correlational selection helps explain a counterintuitive pattern of genetic divergence between the recently derived apple‐ and ancestral hawthorn‐infesting host races ofRhagoletis pomonella(Diptera: Tephritidae). The apple host race terminates diapause and emerges as adults earlier in the season than the hawthorn host race, to coincide with the earlier fruiting phenology of their apple hosts. However, alleles at many loci associated with later emergence paradoxically occur at higher frequencies in sympatric populations of the apple compared to the hawthorn race. We present genomic evidence that historical selection over geographically varying environmental gradients across North America generated genetic correlations between two life history traits, diapause intensity and diapause termination, in the hawthorn host race. Moreover, the loci associated with these life history traits are concentrated in genomic regions in high linkage disequilibrium (LD). These genetic correlations are antagonistic to contemporary selection on local apple host race populations that favours increased initial diapause depth and earlier, not later, diapause termination. Thus, the paradox of apple flies appears due, in part, to pleiotropy or linkage of alleles associated with later adult emergence and increased initial diapause intensity, the latter trait strongly selected for by the earlier phenology of apples. Our results demonstrate how understanding of multivariate trait combinations and the correlative nature of selective forces acting on them can improve predictions concerning adaptive evolution and help explain seemingly counterintuitive patterns of genetic diversity in nature.AbstractAdaptation to novel environments can produce unanticipated genomic responses to selection. Here, we show that latitudinal variation in loci associated with two independent life cycle timing traits supports the hypothesis that historic, geographic selection in the ancestral hawthorn race ofRhagoletis pomonellahas favored trait combinations and shaped genetic variation that is partially antagonistic to the direction of selection on the derived apple race.