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

Author(s):  
Richard P Meisel

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.

2020 ◽  
Author(s):  
Richard P. Meisel

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.


2020 ◽  
Author(s):  
Kiran Adhikari ◽  
Jae Hak Son ◽  
Anna H. Rensink ◽  
Jaweria Jaweria ◽  
Daniel Bopp ◽  
...  

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.


2019 ◽  
Author(s):  
Jae Hak Son ◽  
Tea Kohlbrenner ◽  
Svenia Heinze ◽  
Leo Beukeboom ◽  
Daniel Bopp ◽  
...  

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.


Genetics ◽  
2019 ◽  
pp. genetics.302441.2019 ◽  
Author(s):  
Jae Hak Son ◽  
Tea Kohlbrenner ◽  
Svenia Heinze ◽  
Leo Beukeboom ◽  
Daniel Bopp ◽  
...  

2019 ◽  
Author(s):  
Richard P. Meisel ◽  
Pia U. Olafson ◽  
Kiran Adhikari ◽  
Felix D. Guerrero ◽  
Kranti Konganti ◽  
...  

AbstractSex chromosomes and sex determining genes can evolve fast, with the sex-linked chromosomes often differing between closely related species. A substantial body of population genetics theory has been developed and tested to explain the rapid evolution of sex chromosomes and sex determination. However, we do not know why the sex-linked chromosomes differ between some species pairs yet are relatively conserved in other taxa. Addressing this question will require comparing closely related taxa with conserved and divergent sex chromosomes and sex determination systems to identify biological features that could explain these rate differences. Cytological karyotypes suggest that muscid flies (e.g., house fly) and blow flies are such a taxonomic pair. The sex chromosomes appear to differ across muscid species, whereas they are highly conserved across blow flies. Despite the cytological evidence, we do not know the extent to which muscid sex chromosomes are independently derived along different evolutionary lineages. To address that question, we used genomic data to identify young sex chromosomes in two closely related muscid species, horn fly (Haematobia irritans) and stable fly (Stomoxys calcitrans). We provide evidence that the nascent sex chromosomes of horn fly and stable fly were derived independently from each other and from the young sex chromosomes of the closely related house fly (Musca domestica). We present three different scenarios that could have given rise to the sex chromosomes of horn fly and stable fly, and we describe how the scenarios could be distinguished. Distinguishing between these scenarios in future work could help to identify features of muscid genomes that promote sex chromosome divergence.


Both mouse and man have the common XX/XY sex chromosome mechanism. The X chromosome is of original size (5-6% of female haploid set) and the Y is one of the smallest chromosomes of the complement. But there are species, belonging to a variety of orders, with composite sex chromosomes and multiple sex chromosome systems: XX/XY 1 Y 2 and X 1 X 1 X 2 X 2 /X 1 X 2 Y. The original X or the Y, respectively, have been translocated on to an autosome. The sex chromosomes of these species segregate regularly at meiosis; two kinds of sperm and one kind of egg are produced and the sex ratio is the normal 1:1. Individuals with deviating sex chromosome constitutions (XXY, XYY, XO or XXX) have been found in at least 16 mammalian species other than man. The phenotypic manifestations of these deviating constitutions are briefly discussed. In the dog, pig, goat and mouse exceptional XX males and in the horse XY females attract attention. Certain rodents have complicated mechanisms for sex determination: Ellobius lutescens and Tokudaia osimensis have XO males and females. Both sexes of Microtus oregoni are gonosomic mosaics (male OY/XY, female XX/XO). The wood lemming, Myopus schisticolor , the collared lemming, Dicrostonyx torquatus , and perhaps also one or two species of the genus Akodon have XX and XY females and XY males. The XX, X*X and X*Y females of Myopus and Dicrostonyx are discussed in some detail. The wood lemming has proved to be a favourable natural model for studies in sex determination, because a large variety of sex chromosome aneuploids are born relatively frequently. The dosage model for sex determination is not supported by the wood lemming data. For male development, genes on both the X and the Y chromosomes are necessary.


Genome ◽  
1990 ◽  
Vol 33 (1) ◽  
pp. 80-88 ◽  
Author(s):  
Peter Luykx

A survey of 25 species of lower termites (families Mastotermitidae, Termopsidae, and Kalotermitidae) in Australia revealed that centric fusions are a common theme in karyotype evolution in these insects. All but one of the species studied have a basic XX/XY mechanism of sex determination, secondarily complicated in about a third of a species by centric fusions between autosomes and sex chromosomes. There is no obvious relationship between systematic position and presence or absence of these fusions. Fusions between Y chromosomes and autosomes were more common than fusions between X chromosomes and autosomes, in accord with the prediction of the hypothesis that differential selection between the two sexes is the basis for the spread of sex-linked fusions. The absence of these fusions in many species does not favor the idea that a high degree of sex linkage is a necessary condition for the establishment or maintenance of eusocial behavior in termites. The difference in the mechanism of sex determination from that of cockroaches (XX/XO) argues against the evolutionary derivation of termites from ancestral cockroaches; derivation of both groups from some common ancestor with XX/XY sex determination is more likely.Key words: termites, karotype, evolution, sex chromosomes, Australia.


PEDIATRICS ◽  
1965 ◽  
Vol 35 (5) ◽  
pp. 798-812
Author(s):  
Barton Childs

Sexual reproduction helps to ensure the survival of species by providing opportunities for new combinations of chromosomes in individuals. Organisms have evolved means to accomplish this end by establishing special sex-determining chromosomes which must contain the genes which decide the reproductive attributes of the individual. This decision sets in motion a train of events determining many characteristics related to and stemming from the reproductive sex of the individual which, taken in the aggregate, formulate much of his or her role in life as a male or female. Differences between the sexes are thus created which sometimes appear to be unrelated to reproductive functions, but which are traceable ultimately to them, and some of these differences might represent a hazard to one or other sex, due either to biological or cultural inequalities. Though there are occasional errors and imperfections of sex determination, the mechanism is on the whole a good one and even unsophisticated people are seldom unsure or imprecise in the diagnosis of sex among human beings. But establishment of the sex chromosomes in the forms they have taken in various organisms has resulted in certain consequences which, though they might be beneficial in some instances, certainly contribute to inequalities between the two sexes in ways not necessarily related to the reproductive aspects of sex. The disparity in size between the X and Y chromosomes, for example, means that the homogametic sex (female) is diploid with regard to many loci, while the heterogametic sex (males) must be always haploid. If these chromosomes contain genes which control functions apart from aspects of reproductive sex, even though these be compensated, the genes will be making contributions to aspects of maleness and femaleness which are not accommodated in the usual, practical definition of sex.


2020 ◽  
Author(s):  
Hongbing She ◽  
Zhiyuan Liu ◽  
Zhaosheng Xu ◽  
Helong Zhang ◽  
Feng Cheng ◽  
...  

AbstractSexual reproduction is the primary means of reproduction for the vast majority of macroscopic organisms, including almost all animals and plants. Sex chromosomes are predicted to play a central role in sexual dimorphism. Sex determination in spinach is controlled by a pair of sex chromosomes. However, the mechanisms of sex determination in spinach remain poorly understand. Here, we assembled the genomes of both a female (XX) and a male (YY) individual of spinach, and the genome sizes were 978 Mb with 28,320 predicted genes and 926 Mb with 26,537 predicted genes, respectively. Based on reported sex-linked markers, chromosomes 4 of the female and male genome were defined as the X and Y chromosomes, and a 10 Mb male-specific region of the Y chromosome (MSY) from approximately 95– 105 Mb, was identified that contains abundant transposable elements (92.32%). Importantly, a large-scale inversion of about 13 Mb in length was detected on the X chromosome, corresponding to ~9 Mb and ~4 Mb on the Y chromosome, which were located on both sides of the MSY with two distinct evolutionary strata. Almost all sex-linked/Y-specific markers were enriched on the inversions/MSY, suggesting that the flanked inversions might result in recombination suppression between the X and Y chromosomes to maintain the MSY. Forty-nine genes within the MSY had functional homologs elsewhere in the autosomal region, suggesting movement of genes onto the MSY. The X and Y chromosomes of spinach provide a valuable resource for investigating spinach sex chromosomes evolution from wild to cultivated spinach and also provide a broader understanding of the sex determination model in the Amaranthaceae family.


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