scholarly journals Sexually antagonistic selection promotes genetic divergence between males and females in an ant

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.

Insects ◽  
2021 ◽  
Vol 12 (7) ◽  
pp. 643
Author(s):  
Pierre-Andre Eyer ◽  
Megan N. Moran ◽  
Alexander J. Blumenfeld ◽  
Edward L. Vargo

Sexually antagonistic selection (SAS) occurs when distinct alleles are differentially selected in each sex. In the invasive tawny crazy ant, Nylanderia fulva, a genomic region is under SAS, while the rest of the genome is randomly selected in males and females. In this study, we designed a suite of 15 microsatellite markers to study the origin and evolution of SAS in N. fulva. These SAS markers were polymorphic, with allelic frequencies that are highly different between males and females. All haploid males carry only a subset of the alleles present in the population, while females are reliably heterozygous, with one allele from the male gene pool and a different allele inherited from their mother. In addition, we identified six polymorphic markers not associated with SAS and six markers yielding consistent, yet monomorphic, amplification in the introduced range of this species. Reaction condition optimizations allowed all retained markers to be co-amplified in four PCR mixes. The SAS markers may be used to test for the strength and the extent of the genomic regions under SAS in both the native and introduced ranges of N. fulva, while the set of non-SAS loci may be used to assess the invasion route of this species. Overall, the application of these microsatellite markers will yield insights into the origin and evolution of SAS within and among species of the genus Nylanderia.


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.


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.


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.


2018 ◽  
Author(s):  
Paul A. Saunders ◽  
Samuel Neuenschwander ◽  
Nicolas Perrin

AbstractDeleterious mutations accumulating on non-recombining Y chromosomes can drive XY to XY turnovers, but are thought to prevent XY to ZW turnovers, because the latter require fixation of the ancestral Y. Using individual-based simulations, we explored whether and how a dominant W allele can spread in a young XY system that gradually accumulates deleterious mutations. We also investigated how sexually antagonistic (SA) polymorphism on the ancestral sex chromosomes, and the mechanism controlling X-Y recombination suppression affect these transitions. In contrast with XY to XY turnovers, XY to ZW turnovers cannot be favored by Y chromosome mutation load. If the arrest of X-Y recombination depends on genotypic sex, transitions are strongly hindered by deleterious mutations, and totally suppressed by very small SA cost, because deleterious mutations and female-detrimental SA alleles would have to fix with the Y. If, however, the arrest of X-Y recombination depends on phenotypic sex, X and Y recombine in XY ZW females, allowing for the purge of Y-linked deleterious mutations and loss of the SA polymorphism, causing XY to ZW turnovers to occur at a neutral rate. We generalize our results to other types of turnovers (e.g., triggered by non-dominant sex-determining mutations) and discuss their empirical relevance.


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.


Evolution ◽  
2006 ◽  
Vol 60 (10) ◽  
pp. 2168-2181 ◽  
Author(s):  
Matthew R. Robinson ◽  
Jill G. Pilkington ◽  
Tim H. Clutton-Brock ◽  
Josephine M. Pemberton ◽  
Loeske E.B. Kruuk

2018 ◽  
Author(s):  
Devon E. Pearse ◽  
Nicola J. Barson ◽  
Torfinn Nome ◽  
Guangtu Gao ◽  
Matthew A. Campbell ◽  
...  

AbstractTraits with different fitness optima in males and females cause sexual conflict when they have a shared genetic basis. Heteromorphic sex chromosomes can resolve this conflict and protect sexually antagonistic polymorphisms but accumulate deleterious mutations. However, many taxa lack differentiated sex chromosomes, and how sexual conflict is resolved in these species is largely unknown. Here we present a chromosome-anchored genome assembly for rainbow trout (Oncorhynchus mykiss) and characterize a 56 Mb double-inversion supergene that mediates sex-specific migration through sex-dependent dominance, a mechanism that reduces sexual conflict. The double-inversion contains key photosensory, circadian rhythm, adiposity, and sexual differentiation genes and displays frequency clines associated with latitude and temperature, revealing environmental dependence. Our results constitute the first example of sex-dependent dominance across a large autosomal supergene, a novel mechanism for sexual conflict resolution capable of protecting polygenic sexually antagonistic variation while avoiding the homozygous lethality and deleterious mutation load of heteromorphic sex chromosomes.


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