skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Polygenic response of sex chromosomes to sexual antagonism
Abstract Sexual antagonism occurs when males and females differ in their phenotypic fitness optima but are constrained in their evolution to these optima because of their shared genome. The sex chromosomes, which have distinct evolutionary “interests” relative to the autosomes, are theorized to play an important role in sexually antagonistic conflict. However, the evolutionary responses of sex chromosomes and autosomes have usually been considered independently, that is, via contrasting the response of a gene located on either an X chromosome or an autosome. Here, we study the coevolutionary response of the X chromosome and autosomes to sexually antagonistic selection acting on a polygenic phenotype. We model a phenotype initially under stabilizing selection around a single optimum, followed by a sudden divergence of the male and female optima. We find that, in the absence of dosage compensation, the X chromosome promotes evolution toward the female optimum, inducing coevolutionary male-biased responses on the autosomes. Dosage compensation obscures the female-biased interests of the X, causing it to contribute equally to male and female phenotypic change. We further demonstrate that fluctuations in an adaptive landscape can generate prolonged intragenomic conflict and accentuate the differential responses of the X and autosomes to this conflict.  more » « less
Award ID(s):
2010667
PAR ID:
10516741
Author(s) / Creator(s):
;
Corporate Creator(s):
Editor(s):
Charlesworth, Deborah; Connallon, Tim
Publisher / Repository:
Evolution
Date Published:
Journal Name:
Evolution
Edition / Version:
1
Volume:
78
Issue:
3
ISSN:
0014-3820
Page Range / eLocation ID:
539 to 554
Subject(s) / Keyword(s):
sexual antagonism sexual dimorphism polygenic
Format(s):
Medium: X Size: 2 Other: 0
Size(s):
2
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Sex chromosomes play an outsized role in adaptation and speciation, and thus deserve particular attention in evolutionary genomics. In particular, fusions between sex chromosomes and autosomes can produce neo‐sex chromosomes, which offer important insights into the evolutionary dynamics of sex chromosomes. Here, we investigate the evolutionary origin of the previously reportedDanausneo‐sex chromosome within the tribe Danaini. We assembled and annotated genomes ofTirumala septentrionis(subtribe Danaina),Ideopsis similis(Amaurina),Idea leuconoe(Euploeina) andLycorea halia(Itunina) and identified their Z‐linked scaffolds. We found that theDanausneo‐sex chromosome resulting from the fusion between a Z chromosome and an autosome corresponding to theMelitaea cinxiachromosome (McChr) 21 arose in a common ancestor of Danaina, Amaurina and Euploina. We also identified two additional fusions as the W chromosome further fused with the synteny block McChr31 inI. similisand independent fusion occurred between ancestral Z chromosome and McChr12 inL. halia. We further tested a possible role of sexually antagonistic selection in sex chromosome turnover by analysing the genomic distribution of sex‐biased genes inI. leuconoeandL. halia. The autosomes corresponding to McChr21 and McChr31 involved in the fusions are significantly enriched in female‐ and male‐biased genes, respectively, which could have hypothetically facilitated fixation of the neo‐sex chromosomes. This suggests a role of sexual antagonism in sex chromosome turnover in Lepidoptera. The neo‐Z chromosomes of bothI. leuconoeandL. haliaappear fully compensated in somatic tissues, but the extent of dosage compensation for the ancestral Z varies across tissues and species. 
    more » « less
  2. Sex chromosome dosage compensation is a model to understand the coordinated evolution of transcription; however, the advanced age of the sex chromosomes in model systems makes it difficult to study how the complex regulatory mechanisms underlying chromosome-wide dosage compensation can evolve. The sex chromosomes ofPoecilia pictahave undergone recent and rapid divergence, resulting in widespread gene loss on the male Y, coupled with complete X Chromosome dosage compensation, the first case reported in a fish. The recent de novo origin of dosage compensation presents a unique opportunity to understand the genetic and evolutionary basis of coordinated chromosomal gene regulation. By combining a new chromosome-level assembly ofP. pictawith whole-genome bisulfite sequencing and RNA-seq data, we determine that the YY1 transcription factor (YY1) DNA binding motif is associated with male-specific hypomethylated regions on the X, but not the autosomes. These YY1 motifs are the result of a recent and rapid repetitive element expansion on theP. pictaX Chromosome, which is absent in closely related species that lack dosage compensation. Taken together, our results present compelling support that a disruptive wave of repetitive element insertions carrying YY1 motifs resulted in the remodeling of the X Chromosome epigenomic landscape and the rapid de novo origin of a dosage compensation system. 
    more » « less
  3. Lott, S (Ed.)
    Abstract In species with polygenic sex determination (PSD), multiple male- and female-determining loci on different proto-sex chromosomes segregate as polymorphisms within populations. The extent to which these polymorphisms are at stable equilibria is not yet resolved. Previous work demonstrated that PSD is most likely to be maintained as a stable polymorphism when the proto-sex chromosomes have opposite (sexually antagonistic) fitness effects in males and females. However, these models usually consider PSD systems with only two proto-sex chromosomes, or they do not broadly consider the dominance of the alleles under selection. To address these shortcomings, I used forward population genetic simulations to identify selection pressures that can maintain PSD under different dominance scenarios in a system with more than two proto-sex chromosomes (modeled after the house fly). I found that overdominant fitness effects of male-determining proto-Y chromosomes are more likely to maintain PSD than dominant, recessive, or additive fitness effects. The overdominant fitness effects that maintain PSD tend to have proto-Y chromosomes with sexually antagonistic effects (male-beneficial and female-detrimental). In contrast, dominant fitness effects that maintain PSD tend to have sexually antagonistic multi-chromosomal genotypes, but the individual proto-sex chromosomes do not have sexually antagonistic effects. These results demonstrate that sexual antagonism can be an emergent property of the multi-chromosome genotype without individual sexually antagonistic chromosomes. My results further illustrate how the dominance of fitness effects has consequences for both the likelihood that PSD will be maintained as well as the role sexually antagonistic selection is expected to play in maintaining the polymorphism. 
    more » « less
  4. Genes that originate during evolution are an important source of novel biological functions. Retrogenes are functional copies of genes produced by retroduplication and as such are located in different genomic positions. To investigate retroposition patterns and retrogene expression, we computationally identified interchromosomal retroduplication events in nine portions of the phylogenetic history of malaria mosquitoes, making use of species that do or do not have classical sex chromosomes to test the roles of sex-linkage. We found 40 interchromosomal events and a significant excess of retroduplications from the X chromosome to autosomes among a set of young retrogenes. These young retroposition events occurred within the last 100 million years in lineages where all species possessed differentiated sex chromosomes. An analysis of available microarray and RNA-seq expression data for Anopheles gambiae showed that many of the young retrogenes evolved male-biased expression in the reproductive organs. Young autosomal retrogenes with increased meiotic or postmeiotic expression in the testes tend to be male biased. In contrast, older retrogenes, i.e., in lineages with undifferentiated sex chromosomes, do not show this particular chromosomal bias and are enriched for female-biased expression in reproductive organs. Our reverse-transcription PCR data indicates that most of the youngest retrogenes, which originated within the last 47.6 million years in the subgenus Cellia, evolved non-uniform expression patterns across body parts in the males and females of An. coluzzii. Finally, gene annotation revealed that mitochondrial function is a prominent feature of the young autosomal retrogenes. We conclude that mRNA-mediated gene duplication has produced a set of genes that contribute to mosquito reproductive functions and that different biases are revealed after the sex chromosomes evolve. Overall, these results suggest potential roles for the evolution of meiotic sex chromosome inactivation in males and of sexually antagonistic conflict related to mitochondrial energy function as the main selective pressures for X-to-autosome gene reduplication and testis-biased expression in these mosquito lineages. 
    more » « less
  5. Abstract Sex chromosomes frequently differ from the autosomes in the frequencies of genes with sexually dimorphic or tissue-specific expression. Multiple hypotheses have been put forth to explain the unique gene content of the X chromosome, including selection against male-beneficial X-linked alleles, expression limits imposed by the haploid dosage of the X in males, and interference by the dosage compensation complex on expression in males. Here, we investigate these hypotheses by examining differential gene expression in Drosophila melanogaster following several treatments that have widespread transcriptomic effects: bacterial infection, viral infection, and abiotic stress. We found that genes that are induced (upregulated) by these biotic and abiotic treatments are frequently under-represented on the X chromosome, but so are those that are repressed (downregulated) following treatment. We further show that whether a gene is bound by the dosage compensation complex in males can largely explain the paucity of both up- and downregulated genes on the X chromosome. Specifically, genes that are bound by the dosage compensation complex, or close to a dosage compensation complex high-affinity site, are unlikely to be up- or downregulated after treatment. This relationship, however, could partially be explained by a correlation between differential expression and breadth of expression across tissues. Nonetheless, our results suggest that dosage compensation complex binding, or the associated chromatin modifications, inhibit both up- and downregulation of X chromosome gene expression within specific contexts, including tissue-specific expression. We propose multiple possible mechanisms of action for the effect, including a role of Males absent on the first, a component of the dosage compensation complex, as a dampener of gene expression variance in both males and females. This effect could explain why the Drosophila X chromosome is depauperate in genes with tissue-specific or induced expression, while the mammalian X has an excess of genes with tissue-specific expression. 
    more » « less