Evolution of Autosomal Suppression of the <i>Sex-Ratio</i> Trait in Drosophila

Vaz, Suzana Casaccia; Carvalho, Antonio Bernardo

doi:10.1534/genetics.166.1.265

Cited by 25 publications

(36 citation statements)

References 39 publications

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“…Neutrality of distorter and suppressor alleles resulted in fixation of both, producing even sex ratios, consistent with earlier predictions (Vaz & Carvalho, 2004). High suppressor costs prevented the spread of the suppressor, allowing a sex ratio bias to persist throughout the simulation.…”

Section: Discussionsupporting

confidence: 91%

“…Fitness reductions associated with suppressors have been documented in both dioecious and gynodioecious systems and occur even in the absence of the associated distorter (Bailey, 2002; Wu et al., 1989). Suppressor costs have been further implicated in MSD species by the observation that frequencies of suppressor alleles are lower than predicted by Fisherian selection alone (Hornett et al., 2014; Vaz & Carvalho, 2004). …”

Section: Discussionmentioning

confidence: 99%

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Intragenomic conflict produces sex ratio dynamics that favor maternal sex ratio distorters

Rood

Freedberg

2016

Ecology and Evolution

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Maternal sex ratio distorters (MSDs) are selfish elements that enhance their transmission by biasing their host's sex allocation in favor of females. While previous models have predicted that the female‐biased populations resulting from sex ratio distortion can benefit from enhanced productivity, these models neglect Fisherian selection for nuclear suppressors, an unrealistic assumption in most systems. We used individual‐based computer simulation modeling to explore the intragenomic conflict between sex ratio distorters and their suppressors and explored the impacts of these dynamics on population‐level competition between species characterized by MSDs and those lacking them. The conflict between distorters and suppressors was capable of producing large cyclical fluctuations in the population sex ratio and reproductive rate. Despite fitness costs associated with the distorters and suppressors, MSD populations often exhibited enhanced productivity and outcompeted non‐MSD populations in single and multiple‐population competition simulations. Notably, the conflict itself is beneficial to the success of populations, as sex ratio oscillations limit the competitive deficits associated with prolonged periods of male rarity. Although intragenomic conflict has been historically viewed as deleterious to populations, our results suggest that distorter–suppressor conflict can provide population‐level advantages, potentially helping to explain the persistence of sex ratio distorters in a range of taxa.

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Section: Discussionsupporting

confidence: 91%

Section: Discussionmentioning

confidence: 99%

Intragenomic conflict produces sex ratio dynamics that favor maternal sex ratio distorters

Rood

Freedberg

2016

Ecology and Evolution

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“…At low frequency, a population is female biased and selection on a suppressor for the maintenance of equal sex ratios is strong; but at high frequency, most copies of the distorter are masked, the population sex ratio is close to 50/50, and selection on a suppressor is much weaker. This result explains why selection for Fisherian sex ratios may be inefficient at removing the last few copies of a nonsuppressor allele, even though under a deterministic model, the suppressor will eventually fix (Vaz and Carvalho 2004). In addition, selection is expected to be even less efficient at purging null suppressors if the functional suppressor is dominant, as vanishingly few individuals will express sex-ratio.…”

Section: Discussionmentioning

confidence: 99%

“…Under simple, singlepopulation models of sex-chromosome drive, polymorphism between driving (SR) and standard (ST ) X chromosomes can result from three conditions (Vaz and Carvalho 2004). First, the transmission advantage of an SR chromosome may be balanced by deleterious effects of either the driving locus itself or linked variants.…”

Section: Discussionmentioning

confidence: 99%

“…Because of the impact drive elements have on sex ratios, sexlinked drivers are often referred to as ''sex-ratio distorters '' and the phenotype of skewed progeny sex ratios is termed ''sex-ratio. ' ' The mere transmission advantage of a driver, unless balanced by some detrimental fitness effect or masked by a suppressor, can cause it to sweep through a population in a manner similar to a positively selected mutation (Edwards 1961;Vaz and Carvalho 2004).…”

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Recurrent Selection on the Winters sex-ratio Genes in Drosophila simulans

2010

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Selfish genes, such as meiotic drive elements, propagate themselves through a population without increasing the fitness of host organisms. X-linked (or Y-linked) meiotic drive elements reduce the transmission of the Y (X) chromosome and skew progeny and population sex ratios, leading to intense conflict among genomic compartments. Drosophila simulans is unusual in having a least three distinct systems of X chromosome meiotic drive. Here, we characterize naturally occurring genetic variation at the Winters sex-ratio driver (Distorter on the X or Dox), its progenitor gene (Mother of Dox or MDox), and its suppressor gene (Not Much Yang or Nmy), which have been previously mapped and characterized. We survey three North American populations as well as 13 globally distributed strains and present molecular polymorphism data at the three loci. We find that all three genes show signatures of selection in North America, judging from levels of polymorphism and skews in the site-frequency spectrum. These signatures likely result from the biased transmission of the driver and selection on the suppressor for the maintenance of equal sex ratios. Coalescent modeling indicates that the timing of selection is more recent than the age of the alleles, suggesting that the driver and suppressor are coevolving under an evolutionary ''arms race.'' None of the Winters sex-ratio genes are fixed in D. simulans, and at all loci we find ancestral alleles, which lack the gene insertions and exhibit high levels of nucleotide polymorphism compared to the derived alleles. In addition, we find several ''null'' alleles that have mutations on the derived Dox background, which result in loss of drive function. We discuss the possible causes of the maintenance of presence-absence polymorphism in the Winters sex-ratio genes.

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The fate of a suppressed X-linked meiotic driver: experimental evolution in Drosophila simulans

et al. 2022

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Sex-ratio (SR) meiotic drivers are X-linked selfish genetic elements that promote their own transmission by preventing the production of Y-bearing sperm, which usually lowers male fertility. The spread of SR drivers in populations is expected to trigger the evolution of unlinked drive suppressors, a theoretically predicted co-evolution that has been observed in nature. Once completely suppressed, the drivers are expected either to decline if they still affect the fitness of their carriers, or to evolve randomly and possibly get fixed if the suppressors eliminate their deleterious effects. To explore this issue, we used the Paris sexratio system of Drosophila simulans in which drive results from the joint effect of two elements on the X chromosome: a segmental duplication and a deficient allele of the HP1D2 gene. We set up six experimental populations starting with 2/3 of X chromosomes carrying both elements (X SR ) in a fully suppressing background. We let them evolve independently during almost a hundred generations under strong sexual competition, a condition known to cause the rapid disappearance of unsuppressed Paris X SR in previous experimental populations. In our study, the fate of X SR chromosomes varied among populations, from extinction to their maintenance at a frequency close to the starting one. While the reasons for these variable outcomes are still to be explored, our results show that complete suppression can prevent the demise of an otherwise deleterious X SR chromosome, turning a genetic conflict into cooperation between unlinked loci. Observations in natural populations suggest a contrasting fate of the two elements: disappearance of the duplication and maintenance of deficient HP1D2 alleles.

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Evolution of Autosomal Suppression of the Sex-Ratio Trait in Drosophila

Cited by 25 publications

References 39 publications

Intragenomic conflict produces sex ratio dynamics that favor maternal sex ratio distorters

Intragenomic conflict produces sex ratio dynamics that favor maternal sex ratio distorters

Recurrent Selection on the Winters sex-ratio Genes in Drosophila simulans

The fate of a suppressed X-linked meiotic driver: experimental evolution in Drosophila simulans

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