scholarly journals Stable linkage disequilibrium owing to sexual antagonism

2010 ◽  
Vol 278 (1707) ◽  
pp. 855-862 ◽  
Author(s):  
Francisco Úbeda ◽  
David Haig ◽  
Manus M. Patten

Linkage disequilibrium (LD) is an association between genetic loci that is typically transient. Here, we identify a previously overlooked cause of stable LD that may be pervasive: sexual antagonism. This form of selection produces unequal allele frequencies in males and females each generation, which upon admixture at fertilization give rise to an excess of haplotypes that couple male-beneficial with male-beneficial and female-beneficial with female-beneficial alleles. Under sexual antagonism, LD is obtained for all recombination frequencies in the absence of epistasis. The extent of LD is highest at low recombination and for stronger selection. We provide a partition of the total LD into distinct components and compare our result for sexual antagonism with Li and Nei's model of LD owing to population subdivision. Given the frequent observation of sexually antagonistic selection in natural populations and the number of traits that are often involved, these results suggest a major contribution of sexual antagonism to genomic structure.

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.


2021 ◽  
Vol 288 (1946) ◽  
pp. 20202908
Author(s):  
Leslie M. Kollar ◽  
Scott Kiel ◽  
Ashley J. James ◽  
Cody T. Carnley ◽  
Danielle N. Scola ◽  
...  

A central problem in evolutionary biology is to identify the forces that maintain genetic variation for fitness in natural populations. Sexual antagonism, in which selection favours different variants in males and females, can slow the transit of a polymorphism through a population or can actively maintain fitness variation. The amount of sexually antagonistic variation to be expected depends in part on the genetic architecture of sexual dimorphism, about which we know relatively little. Here, we used a multivariate quantitative genetic approach to examine the genetic architecture of sexual dimorphism in a scent-based fertilization syndrome of the mossCeratodon purpureus.We found sexual dimorphism in numerous traits, consistent with a history of sexually antagonistic selection. The cross-sex genetic correlations (rmf) were generally heterogeneous with many values indistinguishable from zero, which typically suggests that genetic constraints do not limit the response to sexually antagonistic selection. However, we detected no differentiation between the female- and male-specific trait (co)variance matrices (GfandGm, respectively), meaning the evolution of sexual dimorphism may be constrained. The cross-sex cross-trait covariance matrixBcontained both symmetric and asymmetric elements, indicating that the response to sexually antagonistic or sexually concordant selection, and the constraint to sexual dimorphism, are highly dependent on the traits experiencing selection. The patterns of genetic variances and covariances among these fitness components is consistent with partly sex-specific genetic architectures having evolved in order to partially resolve multivariate genetic constraints (i.e. sexual conflict), enabling the sexes to evolve towards their sex-specific multivariate trait optima.


1979 ◽  
Vol 21 (3) ◽  
pp. 391-404 ◽  
Author(s):  
Hans Doll ◽  
A. H. D. Brown

The storage protein hordein contains two major groups of polypeptides which are highly polymorphic in barley, and in its evolutionary progenitor Hordeum spontaneum Koch. Crosses between the two species showed that the complex electrophoretic phenotypes within the two groups of polypeptides are governed by codominant alleles at two corresponding loci, Hor-1 and Hor-2, which are moderately linked (11% ± 2). In natural populations of the wild species, the two complex hordein loci were much more polymorphic than the allozyme loci. Furthermore, the variation at these two loci was highly correlated so that individuals differ from one another at both loci much more frequently than expected from the allele frequencies at the individual loci. Considerable hordein variation was also present in Composite Cross XXI, and there was evidence of reassortment of patterns by the seventeenth generation. Thus the complex hordein loci, with their extreme diversity and linkage disequilibrium, are ideal markers for monitoring evolutionary processes in both natural, or composite cross populations.


2014 ◽  
Author(s):  
Samuel J. Tazzyman ◽  
Jessica K. Abbott

Sexual antagonism occurs when there is a positive intersexual genetic correlation in trait expression but opposite fitness effects of the trait(s) in males and females. As such, it constrains the evolution of sexual dimorphism and may therefore have implications for adaptive evolution. There is currently considerable evidence for the existence of sexually antagonistic genetic variation in laboratory and natural populations, but how sexual antagonism interacts with other evolutionary phenomena is still poorly understood in many cases. Here we explore how self-fertilization and inbreeding affect the maintenance of polymorphism for sexually antagonistic loci. We expected a priori that selfing should reduce the region of polymorphism, since inbreeding reduces the frequency of heterozygotes and speeds fixation. Although this expectation was supported, our results show that there is an interactive effect between the degree of selfing and dominance such that those segregating sexually antagonistic loci that do exist are more likely to be partially dominant. In addition, inbreeding effects may influence population persistence and genomic location of sexually antagonistic loci in separate-sexed organisms.


2014 ◽  
Vol 281 (1776) ◽  
pp. 20132123 ◽  
Author(s):  
Tim Connallon ◽  
Andrew G. Clark

Sexual antagonism, whereby mutations are favourable in one sex and disfavourable in the other, is common in natural populations, yet the root causes of sexual antagonism are rarely considered in evolutionary theories of adaptation. Here, we explore the evolutionary consequences of sex-differential selection and genotype-by-sex interactions for adaptation in species with separate sexes. We show that sexual antagonism emerges naturally from sex differences in the direction of selection on phenotypes expressed by both sexes or from sex-by-genotype interactions affecting the expression of such phenotypes. Moreover, modest sex differences in selection or genotype-by-sex effects profoundly influence the long-term evolutionary trajectories of populations with separate sexes, as these conditions trigger the evolution of strong sexual antagonism as a by-product of adaptively driven evolutionary change. The theory demonstrates that sexual antagonism is an inescapable by-product of adaptation in species with separate sexes, whether or not selection favours evolutionary divergence between males and females.


2019 ◽  
Author(s):  
Garrett McKinney ◽  
Megan V. McPhee ◽  
Carita Pascal ◽  
James E. Seeb ◽  
Lisa W. Seeb

AbstractMany studies exclude loci exhibiting linkage disequilibrium (LD); however, high LD can signal reduced recombination around genomic features such as chromosome inversions or sex-determining regions. Chromosome inversions and sex-determining regions are often involved in adaptation, allowing for the inheritance of co-adapted gene complexes and for the resolution of sexually antagonistic selection through sex-specific partitioning of genetic variants. Genomic features such as these can escape detection when loci with LD are removed; in addition, failing to account for these features can introduce bias to analyses. We examined patterns of LD using network analysis to identify an overlapping chromosome inversion and sex-determining region in chum salmon. The signal of the inversion was strong enough to show up as false population substructure when the entire dataset was analyzed, while the signal of the sex-determining region was only obvious after restricting genetic analysis to the sex chromosome. Understanding the extent and geographic distribution of inversions is now a critically important part of genetic analyses of natural populations. The results of this study highlight the importance of analyzing and understanding patterns of LD in genomic dataset and the perils of ignoring or excluding loci exhibiting LD.


Author(s):  
Leigh W. Simmons

The reproductive interests of males and females will almost always differ, for example over whether to mate and how often, when to produce offspring and how many, or how much to invest in each offspring. Whenever the reproductive interests of males and females differ, opposing selection on males and females to achieve their preferred outcome will generate sexually antagonistic selection. Such sexual conflict is reflected in differences in the appearance and behaviour of the sexes as each evolves to gain the advantage in a fitness ‘arms race’. ‘Sexual conflict’ explores the evolutionary consequences of these arms races in the context of sexual selection as it occurs both before and after mating.


2019 ◽  
Vol 116 (48) ◽  
pp. 24157-24163 ◽  
Author(s):  
Pierre-André Eyer ◽  
Alexander J. Blumenfeld ◽  
Edward L. Vargo

Genetic diversity acts as a reservoir for potential adaptations, yet selection tends to reduce this diversity over generations. However, sexually antagonistic selection (SAS) may promote diversity by selecting different alleles in each sex. SAS arises when an allele is beneficial to one sex but harmful to the other. Usually, the evolution of sex chromosomes allows each sex to independently reach different optima, thereby circumventing the constraint of a shared autosomal genome. Because the X chromosome is found twice as often in females than males, it represents a hot spot for SAS, offering a refuge for recessive male-beneficial but female-costly alleles. Hymenopteran species do not have sex chromosomes; females are diploid and males are haploid, with sex usually determined by heterozygosity at the complementary sex-determining locus. For this reason, their entire genomes display an X-linked pattern, as every chromosome is found twice as often in females than in males, which theoretically predisposes them to SAS in large parts of their genome. Here we report an instance of sexual divergence in the Hymenoptera, a sexually reproducing group that lacks sex chromosomes. In the invasive ant Nylanderia fulva, a postzygotic SAS leads daughters to preferentially carry alleles from their mothers and sons to preferentially carry alleles from their grandfathers for a substantial region (∼3%) of the genome. This mechanism results in nearly all females being heterozygous at these regions and maintains diversity throughout the population, which may mitigate the effects of a genetic bottleneck following introduction to an exotic area and enhance the invasion success of this ant.


Genetics ◽  
1987 ◽  
Vol 115 (2) ◽  
pp. 341-352
Author(s):  
B K Epperson ◽  
R W Allard

ABSTRACT Pairwise linkage disequilibrium values (D) were estimated for 14 allozyme loci in two natural populations of lodgepole pine (Pinus contorta ssp. latifolia). Maternal multilocus genotypes were inferred from samples of (haploid) megagametophytic seed-endosperms. Coupling/repulsion double heterozygotes were distinguished for closely linked pairs of loci. Assays of seven of the loci in seed embryos allowed estimates of D for these loci in the outcross pollen pool (estimates of outcrossing rates indicate no significant departures from random mating in either population). No disequilibrium was observed between unlinked loci in either maternal genotypes or outcross pollen. However, significant disequilibrium was observed within and between gametes for some allelic combinations of four tightly linked loci; the assumption of random association of gamete types within individuals is thus invalid for some loci in lodgepole pine. Possible causes of the observed D were examined using the noncentrality parameter of the general noncentral chi square distribution. We concluded, from estimates of population size, linkage and measurements of population substructure, that neither drift nor population subdivision was responsible for the significant values of D which were observed and that epistatic selection was the most likely cause of the disequilibrium observed.


2018 ◽  
Author(s):  
Mark Hill ◽  
Max Reuter ◽  
Alexander J. Stewart

Males and females have different reproductive roles and are often subject to contrasting selection pressures. This sexual antagonism can lead, at a given locus, to different alleles being favoured in each sex and, consequently, to genetic variation being maintained in a population. Although the presence of antagonistic polymorphisms has been documented across a range of species, their evolutionary dynamics remain poorly understood. Here we study antagonistic selection on gene expression, which is fundamental to sexual dimorphism, via the evolution of regulatory binding sites. We show that for sites longer than 1 nucleotide, polymorphism is maintained only when intermediate expression levels are deleterious to both sexes. We then show that, in a regulatory cascade, polymorphism tends to become displaced over evolutionary time from the target of antagonistic selection to upstream regulators. Our results have consequences for understanding the evolution of sexual dimorphism, and provide specific empirical predictions for the regulatory architecture of genes under antagonistic selection


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