scholarly journals Minimal effects of proto-Y chromosomes on house fly gene expression in spite of evidence that selection maintains stable polygenic sex determination

2019 ◽  
Author(s):  
Jae Hak Son ◽  
Tea Kohlbrenner ◽  
Svenia Heinze ◽  
Leo Beukeboom ◽  
Daniel Bopp ◽  
...  
Keyword(s):  
Gene Expression ◽  
Natural Selection ◽  
Sex Determination ◽  
Developmental Process ◽  
Natural Populations ◽  
House Fly ◽  
Minor Effect ◽  
Master Regulators ◽  
Y Chromosomes ◽  
Polygenic Sex Determination

AbstractSex determination is the developmental process by which organismal sex is established. Sex determination evolves fast, often due to changes in the master regulators at the top of the pathway. In addition, some species are polymorphic for multiple different master regulators within natural populations. Understanding the forces that maintain this polygenic sex determination can be informative of the factors that drive the evolution of sex determination. The house fly, Musca domestica, is a well-suited model to those ends because natural populations harbor male-determining loci on each of the six chromosomes and a bi-allelic female-determiner. Multiple lines of evidence suggest that natural selection maintains polygenic sex determination in house fly. However, previous work found that there are very few sequence differences between proto-Y chromosomes and their homologous X chromosomes. This suggests that there is not much genetic variation upon which natural selection could act to maintain polygenic sex determination in house fly. To address this paradox, we performed RNA-seq experiments that examine the effects of the two most common proto-Y chromosomes on gene expression. We find that the proto-Y chromosomes do indeed have a relatively minor effect on gene expression, as expected based on the minimal X-Y sequence differences. Despite these minimal gene expression differences, we identify some patterns that are consistent with sex-specific selection acting on phenotypic effects of proto-Y chromosomes. Our results suggest that, if natural selection maintains polygenic sex determination in house fly, the phenotypic differences under selection are minor and possibly depend on ecological contexts that were not tested in our experimental design.

scholarly journals Temperature-dependent effects of house fly proto-Y chromosomes on gene expression act independently of the sex determination pathway

2020 ◽  
Author(s):  
Kiran Adhikari ◽  
Jae Hak Son ◽  
Anna H. Rensink ◽  
Jaweria Jaweria ◽  
Daniel Bopp ◽  
...  
Keyword(s):  
Gene Expression ◽  
Sex Determination ◽  
Sex Chromosomes ◽  
Developmental Process ◽  
Natural Populations ◽  
House Fly ◽  
Sexually Dimorphic ◽  
Temperature Dependent ◽  
Y Chromosomes ◽  
Polygenic Sex Determination

AbstractSex determination, the developmental process by which sexually dimorphic phenotypes are established, evolves fast. Species with polygenic sex determination, in which master regulatory genes are found on multiple different proto-sex chromosomes, are informative models to study the evolution of sex determination. House flies are such a model system, with male determining loci possible on all six chromosomes and a female-determiner on one of the chromosomes as well. The distributions of the two most common male-determining proto-Y chromosomes across natural populations suggests that temperature variation is an important selection pressure responsible for maintaining polygenic sex determination in this species. To test that hypothesis, we used RNA-seq to identify temperature-dependent effects of the proto-Y chromosomes on gene expression. We find no evidence for ecologically meaningful temperature-dependent expression of sex determining genes between male genotypes, but we identified hundreds of other genes whose expression depends on the interaction between proto-Y chromosome genotype and temperature. Notably, genes with genotype-by-temperature interactions on expression are not enriched on the proto-sex chromosomes. Moreover, there is no evidence that temperature-dependent expression is driven by chromosome-wide expression divergence between the proto-Y and proto-X alleles. Therefore, if temperature-dependent gene expression is responsible for differences in phenotypes and fitness of proto-Y genotypes across house fly populations, these effects are driven by a small number of temperature-dependent alleles on the proto-Y chromosomes.

scholarly journals The maintenance of polygenic sex determination depends on the dominance of fitness effects which are predictive of the role of sexual antagonism

2020 ◽  
Author(s):  
Richard P. Meisel
Keyword(s):  
Sex Determination ◽  
Sex Chromosomes ◽  
Natural Populations ◽  
House Fly ◽  
Sexual Antagonism ◽  
Antagonistic Selection ◽  
Fitness Effects ◽  
Y Chromosomes ◽  
Sexually Antagonistic Selection ◽  
Polygenic Sex Determination

AbstractIn species with polygenic sex determination, multiple male- and/or female-determining loci on different proto-sex chromosomes segregate as polymorphisms within populations. The extent to which these polymorphisms are stable equilibria is not yet resolved. Previous work demonstrated that polygenic sex determination 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 polygenic sex determination systems with only two proto-sex chromosomes, or they do not broadly consider the dominance of the variants under selection. To address these shortcomings, I used forward population genetic simulations to identify selection pressures that can maintain polygenic sex determination 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 in males are more likely to maintain polygenic sex determination than dominant, recessive, or additive fitness effects. I also found that additive fitness effects that maintain polygenic sex determination have the strongest signatures of sexually antagonistic selection, but there is also some evidence for sexually antagonism when fitness effects of proto-Y chromosomes are dominant or recessive. More generally, these results suggest that the expected effect of sexually antagonistic selection on the maintenance of genetic variation in natural populations will depend on whether the alleles are sex-linked and the dominance of their fitness effects.

scholarly journals Minimal Effects of Proto-Y Chromosomes on House Fly Gene Expression in Spite of Evidence That Selection Maintains Stable Polygenic Sex Determination

Genetics ◽  
2019 ◽  
pp. genetics.302441.2019 ◽  
Author(s):  
Jae Hak Son ◽  
Tea Kohlbrenner ◽  
Svenia Heinze ◽  
Leo Beukeboom ◽  
Daniel Bopp ◽  
...  
Keyword(s):  
Gene Expression ◽  
Sex Determination ◽  
House Fly ◽  
Y Chromosomes ◽  
Polygenic Sex Determination

scholarly journals The maintenance of polygenic sex determination depends on the dominance of fitness effects which are predictive of the role of sexual antagonism

2021 ◽  
Author(s):  
Richard P Meisel
Keyword(s):  
Sex Determination ◽  
Sex Chromosomes ◽  
House Fly ◽  
Sexual Antagonism ◽  
Antagonistic Effects ◽  
Fitness Effects ◽  
Y Chromosomes ◽  
Sexually Antagonistic Selection ◽  
The Individual ◽  
Polygenic Sex Determination

Abstract In species with polygenic sex determination, 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 polygenic sex determination 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 polygenic sex determination 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 polygenic sex determination 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 polygenic sex determination than dominant, recessive, or additive fitness effects. The overdominant fitness effects that maintain polygenic sex determination tend to have proto-Y chromosomes with sexually antagonistic effects (male-beneficial and female-detrimental). In contrast, dominant fitness effects that maintain polygenic sex determination 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 polygenic sex determination will be maintained as well as the role sexually antagonistic selection is expected to play in maintaining the polymorphism.

scholarly journals Gene-level, but not chromosome-wide, divergence between a very young house fly proto-Y chromosome and its homologous proto-X chromosome

2020 ◽  
Author(s):  
Jae Hak Son ◽  
Richard P. Meisel
Keyword(s):  
Gene Expression ◽  
Y Chromosome ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
House Fly ◽  
Evolutionary Divergence ◽  
Y Chromosomes ◽  
Mitochondrial Functions ◽  
Xx Males ◽  
Y Chromosome Evolution

AbstractX and Y chromosomes are usually derived from a pair of homologous autosomes, which then diverge from each other over time. Although Y-specific features have been characterized in sex chromosomes of various ages, the earliest stages of Y chromosome evolution remain elusive. In particular, we do not know whether early stages of Y chromosome evolution consist of changes to individual genes or happen via chromosome-scale divergence from the X. To address this question, we quantified divergence between young proto-X and proto-Y chromosomes in the house fly, Musca domestica. We compared proto-sex chromosome sequence and gene expression between genotypic (XY) and sex-reversed (XX) males. We find evidence for sequence divergence between genes on the proto-X and proto-Y, including five genes with mitochondrial functions. There is also an excess of genes with divergent expression between the proto-X and proto-Y, but the number of genes is small. This suggests that individual proto-Y genes, but not the entire proto-Y chromosome, have diverged from the proto-X. We identified one gene, encoding an axonemal dynein assembly factor (which functions in sperm motility), that has higher expression in XY males than XX males because of a disproportionate contribution of the proto-Y allele to gene expression. The up-regulation of the proto-Y allele may be favored in males because of this gene’s function in spermatogenesis. The evolutionary divergence between proto-X and proto-Y copies of this gene, as well as the mitochondrial genes, is consistent with selection in males affecting the evolution of individual genes during early Y chromosome evolution.

scholarly journals Gene regulation is commonly selected for high plasticity and low noise

2021 ◽  
Author(s):  
Markéta Vlková ◽  
Olin K Silander
Keyword(s):  
Gene Expression ◽  
Gene Regulation ◽  
Natural Selection ◽  
De Novo ◽  
Natural Populations ◽  
Low Noise ◽  
Expression Level ◽  
Direct Selection ◽  
High Plasticity ◽  
Bacterial Gene

Bacteria often respond to dynamically changing environments by regulating gene expression. Despite this regulation being critically important for growth and survival, little is known about how selection shapes gene regulation in natural populations. To better understand the role natural selection plays in shaping bacterial gene regulation, here we compare differences in the regulatory behaviour of naturally segregating promoter variants from Escherichia coli (which have been subject to natural selection) to randomly mutated promoter variants (which have never been exposed to natural selection). We quantify gene expression phenotypes (expression level, plasticity, and noise) for hundreds of promoter variants across multiple environments, and show that segregating promoter variants are enriched for mutations with minimal effects on expression level. In many promoters, we infer that there is strong selection to maintain high levels of plasticity, and direct selection to decrease or increase cell-to-cell variability in expression. Finally, taking an integrated view, we show that across all phenotypes combined, segregating promoter variants are far more phenotypically similar than would be expected given their genetic divergence. This is the consequence of both stabilizing and directional selection acting on individual phenotypes to minimize differences among segregating variants. Taken together, these results expand our knowledge of how gene regulation is affected by natural selection and highlight the power of comparing naturally segregating polymorphisms to de novo random mutations to quantify the action of selection.

scholarly journals Gene-Level, but Not Chromosome-Wide, Divergence between a Very Young House Fly Proto-Y Chromosome and Its Homologous Proto-X Chromosome

2020 ◽  
Author(s):  
Jae Hak Son ◽  
Richard P Meisel
Keyword(s):  
Gene Expression ◽  
Y Chromosome ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
House Fly ◽  
Evolutionary Divergence ◽  
Y Chromosomes ◽  
Mitochondrial Functions ◽  
Xx Males ◽  
Y Chromosome Evolution

Abstract X and Y chromosomes are usually derived from a pair of homologous autosomes, which then diverge from each other over time. Although Y-specific features have been characterized in sex chromosomes of various ages, the earliest stages of Y chromosome evolution remain elusive. In particular, we do not know whether early stages of Y chromosome evolution consist of changes to individual genes or happen via chromosome-scale divergence from the X. To address this question, we quantified divergence between young proto-X and proto-Y chromosomes in the house fly, Musca domestica. We compared proto-sex chromosome sequence and gene expression between genotypic (XY) and sex-reversed (XX) males. We find evidence for sequence divergence between genes on the proto-X and proto-Y, including five genes with mitochondrial functions. There is also an excess of genes with divergent expression between the proto-X and proto-Y, but the number of genes is small. This suggests that individual proto-Y genes, but not the entire proto-Y chromosome, have diverged from the proto-X. We identified one gene, encoding an axonemal dynein assembly factor (which functions in sperm motility), that has higher expression in XY males than XX males because of a disproportionate contribution of the proto-Y allele to gene expression. The upregulation of the proto-Y allele may be favored in males because of this gene’s function in spermatogenesis. The evolutionary divergence between proto-X and proto-Y copies of this gene, as well as the mitochondrial genes, is consistent with selection in males affecting the evolution of individual genes during early Y chromosome evolution.

scholarly journals Polymorphism for Y-Linked Suppressors of sex-ratio in Two Natural Populations of Drosophila mediopunctata

Genetics ◽  
1997 ◽  
Vol 146 (3) ◽  
pp. 891-902 ◽  
Author(s):  
Antonio Bernardo Carvalho ◽  
Suzana Casaccia Vaz ◽  
Louis Bernard Klaczko
Keyword(s):  
Population Genetics ◽  
Population Dynamics ◽  
Natural Selection ◽  
Sex Ratio ◽  
Numerical Simulations ◽  
Natural Populations ◽  
Meiotic Drive ◽  
X Chromosomes ◽  
Variable Expression ◽  
Y Chromosomes

In several Drosophila species there is a trait known as “sex-ratio”: males carrying certain X chromosomes (called “SR”) produce female biased progenies due to X-Y meiotic drive. In Drosophila mediopunctata this trait has a variable expression due to Y-linked suppressors of sex-ratio expression, among other factors. There are two types of Y chromosomes (suppressor and nonsuppressor) and two types of SR chromosomes (suppressible and unsuppressible). Sex-ratio expression is suppressed in males with the SRsuppressible/Ysuppressor genotype, whereas the remaining three genotypes produce female biased progenies. Now we have found that ∼10–20% of the Y chromosomes from two natural populations 1500 km apart are suppressors of sex-ratio expression. Preliminary estimates indicate that Ysuppressor has a meiotic drive advantage of 6% over Ynonsuppressor. This Y polymorphism for a nonneutral trait is unexpected under current population genetics theoly. We propose that this polymorphism is stabilized by an equilibrium between meiotic drive and natural selection, resulting from interactions in the population dynamics of X and Y alleles. Numerical simulations showed that this mechanism may stabilize nonneutral Y polymorphisms such as we have found in D. mediopunctata.

scholarly journals Transcriptome Differences between Alternative Sex Determining Genotypes in the House Fly,Musca domestica

2015 ◽  
Author(s):  
Richard P Meisel ◽  
Jeffrey G Scott ◽  
Andrew G Clark
Keyword(s):  
Gene Expression ◽  
Sex Determination ◽  
Musca Domestica ◽  
Expression Profiles ◽  
Gene Expression Profiles ◽  
House Fly ◽  
Differentially Expressed ◽  
Ancestral State ◽  
Evolutionary Forces ◽  
Sex Determination System

Sex determination evolves rapidly, often because of turnover of the genes at the top of the pathway. The house fly,Musca domestica, has a multifactorial sex determination system, allowing us to identify the selective forces responsible for the evolutionary turnover of sex determination in action. There is a male determining factor,M, on the Y chromosome (YM), which is probably the ancestral state. AnMfactor on the third chromosome (IIIM) has reached high frequencies in multiple populations across the world, but the evolutionary forces responsible for the invasion of IIIMare not resolved. To test if the IIIMchromosome invaded because of sex-specific selection pressures, we used mRNA sequencing to determine if isogenic males that differ only in the presence of the YMor IIIMchromosome have different gene expression profiles. We find that more genes are differentially expressed between YMand IIIMmales in testis than head, and that genes with male-biased expression are most likely to be differentially expressed between YMand IIIMmales. We additionally find that IIIMmales have a "masculinized" gene expression profile, suggesting that the IIIMchromosome has accumulated an excess of male-beneficial alleles because of its male-limited transmission. These results are consistent with the hypothesis that sex-specific selection acts on alleles linked to the male-determining locus driving evolutionary turnover in the sex determination pathway.

Sign in / Sign up

Export Citation Format

Share Document