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.

Explore Research Products in the PAR
It may take a few hours for recently added research products to appear in PAR search results.


Title: Fitness consequences of a non-recombining sex-ratio drive chromosome can explain its prevalence in the wild
Understanding the pleiotropic consequences of gene drive systems on host fitness is essential to predict their spread through a host population. Here, we study sex-ratio (SR) X-chromosome drive in the fly Drosophila recens , where SR causes the death of Y-bearing sperm in male carriers. SR males only sire daughters, which all carry SR, thus giving the chromosome a transmission advantage. The prevalence of the SR chromosome appears stable, suggesting pleiotropic costs. It was previously shown that females homozygous for SR are sterile, and here, we test for additional fitness costs of SR. We found that females heterozygous for SR have reduced fecundity and that male SR carriers have reduced fertility in conditions of sperm competition. We then use our fitness estimates to parametrize theoretical models of SR drive and show that the decrease in fecundity and sperm competition performance can account for the observed prevalence of SR in natural populations. In addition, we found that the expected equilibrium frequency of the SR chromosome is particularly sensitive to the degree of multiple mating and performance in sperm competition. Together, our data suggest that the mating system of the organism should be carefully considered during the development of gene drive systems.  more » « less
Award ID(s):
1737824 1149350
PAR ID:
10277279
Author(s) / Creator(s):
;
Date Published:
Journal Name:
Proceedings of the Royal Society B: Biological Sciences
Volume:
286
Issue:
1917
ISSN:
0962-8452
Page Range / eLocation ID:
20192529
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; (, Molecular Ecology)
    Abstract Selfish genetic elements that manipulate gametogenesis to achieve a transmission advantage are known as meiotic drivers.Sex‐ratioX chromosomes (SR) are meiotic drivers that prevent the maturation of Y‐bearing sperm in male carriers to result in the production of mainly female progeny. The spread of an SR chromosome can affect host genetic diversity and genome evolution, and can even cause host extinction if it reaches sufficiently high prevalence. Meiotic drivers have evolved independently many times, though only in a few cases is the underlying genetic mechanism known. In this study we use a combination of transcriptomics and population genetics to identify widespread expression differences between the standard (ST) andsex‐ratio(SR) X chromosomes of the flyDrosophila neotestacea.We found the X chromosome is enriched for differentially expressed transcripts and that many of these X‐linked differentially expressed transcripts had elevatedKa/Ksvalues between ST and SR, indicative of potential functional differences. We identified a set of candidate transcripts, including a testis‐specific, X‐linked duplicate of the nuclear transport geneimportin‐α2that is overexpressed in SR.We find suggestions of positive selection in the lineage leading to the duplicate and that its molecular evolutionary patterns are consistent with relaxed purifying selection in ST. As these patterns are consistent with involvement in the mechanism of drive in this species, this duplicate is a strong candidate worthy of further functional investigation. Nuclear transport may be a common target for genetic conflict, as the mechanism of the autosomalSegregation Distorterdrive system inD. melanogasterinvolves the same pathway. 
    more » « less
  2. ; ; ; ; (, bioRxiv)
    Abstract Gut microbiomes provide numerous physiological benefits for host animals. The role of bacterial members of microbiomes in host physiology is well-documented. However, much less is known about the contributions and interactions of fungal members of the microbiome even though fungi are significant components of many microbiomes, including those of humans and insects. Here, we used antibacterial and antifungal drugs to manipulate the gut microbiome of a Hawaiian picture-wingDrosophilaspecies,D. grimshawi, and identified distinct, sex-specific roles for the bacteria and fungi in microbiome community stability and reproduction. Female oogenesis, fecundity and mating drive were significantly diminished when fungal communities were suppressed. By contrast, male fecundity was more strongly affected by bacterial but not fungal populations. For males and females, suppression of both bacteria and fungi severely reduced fecundity and altered fatty acid levels and composition, implicating the importance of interkingdom interactions on reproduction and lipid metabolism. Overall, our results reveal that bacteria and fungi have distinct, sexually-dimorphic effects on host physiology and interkingdom dynamics in the gut help to maintain microbiome community stability and enhance reproduction. 
    more » « less
  3. ; ; ; ; ; ; (, bioRxiv)
    A major goal in evolutionary biology is to understand how natural variation is maintained in sexually selected and sexually dimorphic traits. Hypotheses to explain genetic variation in sexually selected traits include context-dependent fitness effects, epistatic interactions, and pleiotropic constraints. The house fly, Musca domestica, is a promising system to investigate how these factors affect polymorphism in sexually selected traits. Two common Y chromosomes (YM and IIIM) segregate as stable polymorphisms in natural house fly populations, appear to be locally adapted to different thermal habitats, and differentially affect male mating success. Here, we perform a meta-analysis of RNA-seq data which identifies genes encoding odorant binding proteins (in the Obp56h family) as differentially expressed between the heads of males carrying YM and IIIM Differential expression of Obp56h has been associated with variation in male mating behavior in Drosophila melanogaster. We find differences in male mating behavior between house flies carrying the Y chromosomes that are consistent with the relationship between male mating behavior and expression of Obp56h in D. melanogaster. We also find that male mating behaviors in house fly are affected by temperature, and the same temperature differentials further affect the expression of Obp56h genes. However, we show that temperature-dependent effects cannot explain the maintenance of genetic variation for male mating behavior in house fly. Using a network analysis and allele-specific expression measurements, we find evidence that the house fly IIIM chromosome is a trans regulator of Obp56h gene expression. Moreover, we find that Obp56h disproportionately affects the expression of genes on the D. melanogaster chromosome that is homologous to the house fly IIIM chromosome. This provides evidence for a conserved trans regulatory loop involving Obp56h expression that affects male mating behavior in flies. The complex regulatory architecture controlling Obp56h expression suggests that variation in male mating behavior could be maintained by epistasis or pleiotropic constraints. 
    more » « less
  4. ; ; ; ; ; ; ; ; ; ; et al (, Evolution)
    Abstract It remains unclear how variation in the intensity of sperm competition shapes phenotypic and molecular evolution across clades. Mice and rats in the subfamily Murinae are a rapid radiation exhibiting incredible diversity in sperm morphology and production. We combined phenotypic and genomic data to perform phylogenetic comparisons of male reproductive traits and genes across 78 murine species. We identified several shifts towards smaller relative testes mass (RTM), presumably reflecting reduced sperm competition. Several sperm traits were associated with RTM, suggesting that mating system evolution selects for convergent suites of traits related to sperm competitive ability. We predicted that sperm competition would also drive more rapid molecular divergence in species with large testes. Contrary to this, we found that many spermatogenesis genes evolved more rapidly in species with smaller RTM due to relaxed purifying selection. While some reproductive genes evolved rapidly under recurrent positive selection, relaxed selection played a greater role in underlying rapid evolution in small testes species. Our work demonstrates that postcopulatory sexual selection can impose strong purifying selection shaping the evolution of male reproduction and that broad patterns of molecular evolution may help identify genes that contribute to male fertility. 
    more » « less
  5. ; (, Evolution Letters)
    Abstract In contrast to sexual selection on traits that affect interactions between the sexes before mating, little theoretical research has focused on the coevolution of postmating traits via cryptic female choice (when females bias fertilization toward specific males). We used simulation models to ask (a) whether and, if so, how nondirectional cryptic female choice (female-by-male interactions in fertilization success) causes deviations from models that focus exclusively on male-mediated postmating processes, and (b) how the risk of sperm competition, the strength of cryptic female choice, and tradeoffs between sperm number and sperm traits interact to influence the coevolutionary dynamics between cryptic female choice and sperm traits. We found that incorporating cryptic female choice can result in males investing much less in their ejaculates than predicted by models with sperm competition only. We also found that cryptic female choice resulted in the evolution of genetic correlations between cryptic female choice and sperm traits, even when the strength of cryptic female choice was weak, and the risk of sperm competition was low. This suggests that cryptic female choice may be important even in systems with low multiple mating. These genetic correlations increased with the risk of sperm competition and as the strength of cryptic female choice increased. When the strength of cryptic female choice and risk of sperm competition was high, extreme codivergence of sperm traits and cryptic female choice preference occurred even when the sperm trait traded off with sperm number. We also found that male traits lagged behind the evolution of female traits; this lag decreased with increasing strength of cryptic female choice and risk of sperm competition. Overall, our results suggest that cryptic female choice deserves more attention theoretically and may be driving trait evolution in ways just beginning to be explored. 
    more » « less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email