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

Abstract

Allele frequencies can shift rapidly within natural populations. Under certain conditions, repeated rapid allele frequency shifts can lead to the long‐term maintenance of polymorphism. In recent years, studies of the model insect Drosophila melanogaster have suggested that this phenomenon is more common than previously believed and is often driven by some form of balancing selection, such as temporally fluctuating or sexually antagonistic selection. Here we discuss some of the general insights into rapid evolutionary change revealed by large‐scale population genomic studies, as well as the functional and mechanistic causes of rapid adaptation uncovered by single‐gene studies. As an example of the latter, we consider a regulatory polymorphism of the D. melanogaster fezzik gene. Polymorphism at this site has been maintained at intermediate frequency over an extended period of time. Regular observations from a single population over a period of 7 years revealed significant differences in the frequency of the derived allele and its variance across collections between the sexes. These patterns are highly unlikely to arise from genetic drift alone or from the action of sexually antagonistic or temporally fluctuating selection individually. Instead, the joint action of sexually antagonistic and temporally fluctuating selection can best explain the observed rapid and repeated allele frequency shifts. Temporal studies such as those reviewed here further our understanding of how rapid changes in selection can lead to the long‐term maintenance of polymorphism as well as improve our knowledge of the forces driving and limiting adaptation in nature.

A cosmopolitan inversion facilitates seasonal adaptation in overwintering Drosophila

“…Differentiating between these adaptive and demographic hypotheses will require functional validation of the putative drivers of the sweeps (e.g. Glaser-Schmitt et al 2023 ). Functional evidence will be important for testing whether seasonal adaptation in In(2L)t is “fine-tuned” by young, habitat-specific alleles.…”

Inversions Can Accumulate Balanced Sexual Antagonism: Evidence from Simulations and Drosophila Experiments

“…D. melanogaster mating involves a male display performance and female acceptance or rejection. A number of experimental evolution studies (Rice 1992 ;Rice 1996 ;Audet et al 2023) and genetic studies (Innocenti and Morrow 2010 ;Cheng and Kirkpatrick 2016 ;Glaser-Schmitt et al 2023 ) have confirmed the prevalence of sexually antagonistic loci in D. melanogaster. Pleiotropic alleles that trade off between survival and male display quality may be the simplest case of antagonism to consider for a model of balancing selection, and one highly relevant to the biology of D. melanogaster.…”

Inversions Can Accumulate Balanced Sexual Antagonism: Evidence from Simulations andDrosophilaExperiments

“…melanogaster mating involves a male display performance and female acceptance or rejection. A number of experimental evolution studies (Rice 1992;Rice 1996;Audet et al 2023) and genetic studies (Innocenti and Morrow 2010;Cheng and Kirkpatrick 2016;Glaser-Schmitt et al 2023) have confirmed the prevalence of sexually antagonistic loci in D. melanogaster. Pleiotropic alleles that trade off between survival and male display quality may be the simplest case of antagonism to consider for a model of balancing selection, and one highly relevant to the biology of D. melanogaster.…”