Distinct signals of clinal and seasonal allele frequency change at eQTLs in Drosophila melanogaster

Abstract

Populations of short-lived organisms can respond to spatial and temporal environmental heterogeneity through local adaptation.Local adaptation can be reflected on both phenotypic and genetic levels, and it has been documented in many organisms. Although complex fitness-related phenotypes have been shown to vary across latitudinal clines and seasons in similar ways in Drosophila melanogaster populations, the comparative signals of local adaptation across space and time remain poorly understood. Here, we examined patterns of allele frequency change across a latitudinal cline and between seasons at previously reported expression quantitative trait loci (eQTLs). We divided eQTLs into groups by using differential expression profiles of fly populations collected across latitudinal clines or exposed to different environmental conditions. In general, we find that eQTLs are enriched for clinally varying polymorphisms, and that these eQTLs change in frequency in concordant ways across the cline and in response to starvation and chill-coma. The enrichment of eQTLs among seasonally varying polymorphisms is more subtle, and the direction of allele frequency change at eQTLs appears to be somewhat idiosyncratic. Taken together, we suggest that clinal adaptation at eQTLs is at least partially distinct from seasonal adaptation.

How predictable is rapid evolution?

“…It is possible that alleles in different genes might produce a similar phenotype in these polygenic traits; it cannot be assumed that the same alleles undergo selection each year to produce the complex trait. This is consistent with the idiosyncratic effects of seasonal expression quantitate trait loci (QTL) across years (45). Additionally, interactions among seasonal alleles can result in positive epistasis and increase trait values in non-additive ways, but may also result in negative epistasis that purges certain allele combinations from the population (29).…”

A cosmopolitan inversion facilitates seasonal adaptation in overwintering Drosophila

“…6b ). We refer to this statistic as the “directionality” statistic following Erickson et al (2020) , Machado et al (2021) , and Yu and Bergland (2022) . Directionality scores are calculated by comparing the sign of the regression coefficients for the 2 models.…”

“…For example, variations in stress tolerance and life history enable some individuals to better survive the winter months while others more effectively exploit resources in the growing season ( Behrman et al 2015 ; Rajpurohit et al 2018 ; Erickson et al 2020 ; cf. Yu and Bergland 2022 ). These observations suggest that seasonal adaptation operates through a resource-allocation tradeoff between reproduction and survival that is also mirrored across latitudinal gradients ( Schmidt and Conde 2006 ).…”

Rapid evolutionary change, constraints and the maintenance of polymorphism in natural populations of Drosophila melanogaster

“…When spatially varying selection occurs, genetic variation can be maintained between populations as local adaptation occurs across the species' range. In Drosophila populations, latitudinal clines in allozyme, inversion and allele frequency have been well-documented and are thought to be maintained by spatially varying selection (Anderson et al, 2005;Durmaz et al, 2018;Durmaz et al, 2019;Kapun et al, 2016;Lange et al, 2022;Oakeshott et al, 1982;Verrelli & Eanes, 2001;Yu & Bergland, 2022). Indeed, inversions are thought to be particularly important in the maintenance of genetic variation as they prevent linked adaptive variants from recombining away from one another, sometimes leading to the evolution of so-called 'supergenes' (reviewed in Llaurens et al, 2017).…”