Analysing quantitative trait loci of sexual antagonism in fruitflies

Lead Research Organisation: University College London
Department Name: Genetics Evolution and Environment

Abstract

Evolutionary biologists have long been fascinated by the differences between the sexes. Males and females can differ profoundly in appearance and behaviour, in the example of the mallard so much so that the sexes were initially described as members of different species. Past research has shown that sexual dimorphism has arisen in response to differing male and female reproductive roles. Females usually produce large and energetically costly eggs. Their reproductive performance, or 'fitness', is therefore limited by their ability to acquire resources and survive. Males, in contrast, produce large amounts of tiny and cheap sperm. Accordingly, their fitness is in most cases limited by their ability to attract mates, which can involve bright colouration and extravagant displays or exaggerated weaponry to defend a territory of high quality. While it is understood why the sexes differ, the question of how males and females diverge has not been resolved. The underlying problem is that males and females cannot evolve independently because the sexes generally share almost all of their genes. Thus, any difference between the sexes is not caused by a different content of genes, but rather relies on a different subset of genes being used in males and females. However, recent results indicate that the evolution of this differential use of genes is incomplete. Studies in a variety of organisms, ranging from fruitflies to deer, have demonstrated that genomes that improve performance in males often tend to decrease performance in females and vice versa. This data indicates that there are genes that affect male and female performance in opposite directions but are not differentially expressed in the two sexes. So far, these so-called sexually antagonistic genes have only been indirectly inferred by comparing the performance of males and females that are members of the same family (and hence can be expected to share a proportion of their genes). Nothing is known about the identity of the genes that cause antagonism, or their function in the organism or how they evolve. This project will fill this gap in our knowledge. We will identify the genomic regions that have opposite effects on male and female performance and determine where they are located and which genes they contain. Further, we will investigate to what extent sexual antagonism can prevent genes that code for high performance in one sex from spreading through the population, due to their negative effect on the other sex. Finally, we will study the patterns of DNA evolution of loci involved in antagonism in order identify the exact nucleotide sites responsible for differences in sex-specific performance. Doing so will allow us to infer for how long sexual antagonism has persisted at these loci. By addressing these multiple aspects, our project will provide information that will help us to understand the factors that prevent some genes from being differentially expressed. Thus we will deepen our general understanding of how differences between males and females can evolve.

Publications

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Description Males and females of the same species can differ profoundly in appearance and behaviour. Such 'sexual dimorphism' has arisen in response to differing male and female reproductive roles. Females usually produce large and energetically costly eggs and their reproductive performance is typically limited by their ability to acquire resources and survive. Males, in contrast, produce large amounts of cheap sperm are limited by their ability to attract mates. As a consequence of the different reproductive roles of males and females, homologous traits in the two sexes are frequently under divergent selection.

A response to opposing sex-specific selection pressures towards dimorphism is, however, not straightforward. In the vast majority of species, males and females share all or almost all of their genome and therefore cannot evolve independently. In this case, divergent selection can favour genetic variants that are beneficial to one sex (moving the trait values closer to the optimum, but detrimental to the other (moving the trait value away from the optimum. Studies in a variety of organisms, ranging from plants over fruitflies to deer, have demonstrated that despite such 'sexually antagonistic' variation is widespread in populations, despite the dimorphism observed in these species. This indicates that in many cases the evolution of dimorphism is incomplete and constrained by the genetic coupling between sexes.

So far, the existence of sexually antagonistic variation had only be inferred using quantitative genetic approaches, by comparing the performance of males and females from different genotypes. Nothing was known about the identity of the genes that cause antagonism, their function or how they evolve. This project has filled this gap in our knowledge. Using a combination of experimentation, population genomics and bioinformatics, we have for the first time identified the loci underlying sexual antagonism in a population of the fruitfly Drosophila melanogaster. We use sex-specific fitness data from 202 fully sequenced hemiclonal Drosophila melanogaster fly lines to perform a genome-wide association study (GWAS) of sexual antagonism. We identified approximately 230 chromosomal clusters of candidate antagonistic single nucleotide polymorphisms (SNPs). In contradiction to classic theory, we find no clear evidence that the X chromosome is a hot spot for sexually antagonistic variation. Characterising antagonistic SNPs functionally, we find a large excess of missense variants but little enrichment in terms of gene function. We also assess the evolutionary persistence of antagonistic variants by examining extant polymorphism in wild D. melanogaster populations and closely related species. Remarkably, antagonistic variants are associated with multiple signatures of balancing selection across the D. melanogaster distribution range and in their sister species D. simulans, indicating widespread and evolutionarily persistent (about 1 million
years) genomic constraints on the evolution of sexual dimorphism. Based on our results, we
propose that antagonistic variation accumulates because of constraints on the resolution of sexual conflict over protein coding sequences, thus contributing to the long-term maintenance of heritable fitness variation.
Exploitation Route The results we have generated provide avenues for further study of sexual antagonism. In particular, we are planning to pursue the experimental verification of our candidate genes. In parallel, we will conduct further comparative analyses to investigate the dynamics and mechanisms of resolving sexual antagonism over longer timescales.
Sectors Agriculture

Food and Drink

Environment