Fitness consequences of the selfish supergene <i>Segregation Distorter</i>

Wong, Heidi W. S.; Holman, Luke

doi:10.1111/jeb.13549

Cited by 9 publications

(11 citation statements)

References 36 publications

(82 reference statements)

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“…Selfish genetic elements are difficult to observe, because they either spread to fixation or are repressed by other genes (20,31). The ones that persist are often recessive lethal or nearlethal, so that negative frequency-dependent selection prevents the fixation of the driving allele (14,19,22,24). In the Alpine silver ant, viable homozygotes are commonly found for both haplotypes of the social supergene (5,30).…”

Section: Discussionmentioning

confidence: 99%

“…Selfish genetic elements that distort Mendelian transmission, here defined as the expected 1:1 transmission ratio of each allele from a heterozygous parent to adult offspring, typically arise through tight linkage of a distorter and target locus, followed by further accumulation of enhancer loci (14,15). Therefore, large non-recombining genomic regions are likely not only to control complex phenotypes, but also to ally against other genes and cause transmission ratio distortion (12,(16)(17)(18)(19)(20). Such transmission ratio distortion may thus play a major role in the initial increase in frequency and later maintenance of supergenes.…”

Section: Introductionmentioning

confidence: 99%

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Maternal effect killing by a supergene controlling ant social organization

Avril

Purcell

Béniguel

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Supergenes underlie striking polymorphisms in nature, yet the evolutionary mechanisms by which they arise and persist remain enigmatic. These clusters of linked loci can spread in populations because they captured coadapted alleles or by selfishly distorting the laws of Mendelian inheritance. Here, we show that the supergene haplotype associated with multiple-queen colonies in Alpine silver ants is a maternal effect killer. All eggs from heterozygous queens failed to hatch when they did not inherit this haplotype. Hence, the haplotype specific to multiple-queen colonies is a selfish genetic element that enhances its own transmission by causing developmental arrest of progeny that do not carry it. At the population level, such transmission ratio distortion favors the spread of multiple-queen colonies, to the detriment of the alternative haplotype associated with single-queen colonies. Hence, selfish gene drive by one haplotype will impact the evolutionary dynamics of alternative forms of colony social organization. This killer hidden in a social supergene shows that large nonrecombining genomic regions are prone to cause multifarious effects across levels of biological organization.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Maternal effect killing by a supergene controlling ant social organization

Avril

Purcell

Béniguel

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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“…Contrary to this prediction, SD was only found on 0-8% of second chromosomes in a sample of wild D. melanogaster populations [6]. A possible explanation for this is that some variants of the SD allele accumulate harmful, recessive mutations causing lethality, sterility or greatly reduced fitness in SD/SD homozygotes [8,9]. These recessive mutations impose negative frequency-dependent selection on SD: as SD becomes more common, the within-individual benefits of distortion are increasingly offset by the costs to SD alleles in homozygotes, creating a balanced polymorphism of SD and non-distorting alleles.…”

Section: Introductionmentioning

confidence: 79%

“…This assumption simplifies the model considerably, and reflects reality for at least two of the SD variants [the third has low but non-zero fitness in homozygotes; 9]. Removing this assumption would result in elevated allele frequencies for SD, while modelling a viability cost to SD/+ individuals would lower the frequency of SD [see9,26].After removing non-viable genotypes, the population matures to adulthood and breeds. We implement precopulatory sexual selection on males via a parameter Sprecop.…”

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confidence: 99%

Sexual selection can partly explain low frequencies of Segregation Distorter alleles

2021

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The Segregation Distorter ( SD ) allele found in Drosophila melanogaster distorts Mendelian inheritance in heterozygous males by causing developmental failure of non- SD spermatids, such that greater than 90% of the surviving sperm carry SD . This within-individual advantage should cause SD to fix, and yet SD is typically rare in wild populations. Here, we explore whether this paradox can be resolved by sexual selection, by testing if males carrying three different variants of SD suffer reduced pre- or post-copulatory reproductive success. We find that males carrying the SD allele are just as successful at securing matings as control males, but that one SD variant ( SD-5 ) reduces sperm competitive ability and increases the likelihood of female remating. We then used these results to inform a theoretical model; we found that sexual selection could limit SD to natural frequencies when sperm competitive ability and female remating rate equalled the values observed for SD-5 . However, sexual selection was unable to explain natural frequencies of the SD allele when the model was parameterized with the values found for two other SD variants, indicating that sexual selection alone is unlikely to explain the rarity of SD .

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“…Incorporating multiple components of fitness into models of meiotic drive dynamics is a promising route to understand how drivers are maintained at an intermediate frequency in the wild. In addition to our system, this approach has helped to explain the prevalence of centromere drive in Mimulus plants [40], Ab10 in maize [41], t-haplotype in mouse [42], Segregation Distorter in Drosophila melanogaster [43] and SR drive in D. pseudoobscura [12]. These studies indicate that estimating all of the fitness consequences of natural gene drivers and the parameters that contribute to their prevalence is critical when developing synthetic gene drive systems (e.g.…”

Section: Discussionmentioning

confidence: 99%

Fitness consequences of a non-recombiningsex-ratiodrive chromosome can explain its prevalence in the wild

Dyer

Hall

2019

Proc. R. Soc. B.

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Understanding the pleiotropic consequences of gene drive systems on host fitness is essential to predict their spread through a host population. Here, we study sex-ratio (SR) X-chromosome drive in the fly Drosophila recens , where SR causes the death of Y-bearing sperm in male carriers. SR males only sire daughters, which all carry SR, thus giving the chromosome a transmission advantage. The prevalence of the SR chromosome appears stable, suggesting pleiotropic costs. It was previously shown that females homozygous for SR are sterile, and here, we test for additional fitness costs of SR. We found that females heterozygous for SR have reduced fecundity and that male SR carriers have reduced fertility in conditions of sperm competition. We then use our fitness estimates to parametrize theoretical models of SR drive and show that the decrease in fecundity and sperm competition performance can account for the observed prevalence of SR in natural populations. In addition, we found that the expected equilibrium frequency of the SR chromosome is particularly sensitive to the degree of multiple mating and performance in sperm competition. Together, our data suggest that the mating system of the organism should be carefully considered during the development of gene drive systems.

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Fitness consequences of the selfish supergene Segregation Distorter

Abstract: This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as

Cited by 9 publications

References 36 publications

Maternal effect killing by a supergene controlling ant social organization

Maternal effect killing by a supergene controlling ant social organization

Sexual selection can partly explain low frequencies of Segregation Distorter alleles

Fitness consequences of a non-recombiningsex-ratiodrive chromosome can explain its prevalence in the wild

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