Sexually Antagonistic Zygotic Drive: A New Form of Genetic Conflict between the Sex Chromosomes

Friberg, Urban; Rice, William R.

doi:10.1101/cshperspect.a017608

Cited by 10 publications

(10 citation statements)

References 28 publications

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“…; Wilkinson et al . ; Gell & Reenan ; Friberg & Rice ; Zanders & Malik ). However, this scenario is unlikely because the recurrent pattern of segregation distortion occurs in the parental male line (i.e.…”

Section: Discussionmentioning

confidence: 99%

“…An alternative hypothesis is meiotic drive, in which a selfish element biases Mendelian segregation by moving away from dead-end polar bodies into the functional egg during oogenesis (Johns et al 2005;Wilkinson et al 2006;Gell & Reenan 2013;Friberg & Rice 2014;Zanders & Malik 2015). However, this scenario is unlikely because the recurrent pattern of segregation distortion occurs in the parental male line (i.e.…”

Section: Molecular Mechanisms Causing Transmission Ratio Distortionmentioning

confidence: 99%

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Sex‐specific allelic transmission bias suggests sexual conflict at MC1R

et al. 2016

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Sexual conflict arises when selection in one sex causes the displacement of the other sex from its phenotypic optimum, leading to an inevitable tension within the genome - called intralocus sexual conflict. Although the autosomal melanocortin-1-receptor gene (MC1R) can generate colour variation in sexually dichromatic species, most previous studies have not considered the possibility that MC1R may be subject to sexual conflict. In the barn owl (Tyto alba), the allele MC1RWHITE is associated with whitish plumage coloration, typical of males, and the allele MC1RRUFOUS is associated with dark rufous coloration, typical of females, although each sex can express any phenotype. Because each colour variant is adapted to specific environmental conditions, the allele MC1RWHITE may be more strongly selected in males and the allele MC1RRUFOUS in females. We therefore investigated whether MC1R genotypes are in excess or deficit in male and female fledglings compared with the expected Hardy-Weinberg proportions. Our results show an overall deficit of 7.5% in the proportion of heterozygotes in males and of 12.9% in females. In males, interannual variation in assortative pairing with respect to MC1R explained the year-specific deviations from Hardy-Weinberg proportions, whereas in females, the deficit was better explained by the interannual variation in the probability of inheriting the MC1RWHITE or MC1RRUFOUS allele. Additionally, we observed that sons inherit the MC1RRUFOUS allele from their fathers on average slightly less often than expected under the first Mendelian law. Transmission ratio distortion may be adaptive in this sexually dichromatic species if males and females are, respectively, selected to display white and rufous plumages.

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Section: Discussionmentioning

confidence: 99%

Section: Molecular Mechanisms Causing Transmission Ratio Distortionmentioning

confidence: 99%

Sex‐specific allelic transmission bias suggests sexual conflict at MC1R

et al. 2016

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“…An increase of abortion frequency in mothers of lesbians has indeed been observed (Ellis and Blanchard 2001). Such a SA zygotic drive would, in any case, be expected to be temporary, because, although lacking compensatory effects, it would be rapidly repressed by Fisherian sex-ratio selection (see Friberg and Rice 2014). Rice et al (2008) indicate such a mechanism could account for some of the asymmetries reported for HS females by Pattatucci and Hamer (1995), showing elevated frequencies of HS in female relatives whose fathers shared the same Y chromosome, as nieces from paternal uncles.…”

Section: Candidate Selection Mechanisms For Female Hsmentioning

confidence: 94%

“…In particular, to account for some peculiar patterns observed within the families of HS females, it has been hypothesized that sexual conflict be at play through (epi)genetic factors known as sexually antagonistic zygotic drive, which might contribute to the transmission (Rice et al 2008; see also Friberg and Rice 2014). This would posit sexual conflict as a basic selection mechanism also for HS in females.…”

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confidence: 99%

Human Homosexuality: A Paradigmatic Arena for Sexually Antagonistic Selection?

Ciani

Battaglia

Zanzotto

2015

Cold Spring Harb Perspect Biol

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Sexual conflict likely plays a crucial role in the origin and maintenance of homosexuality in our species. Although environmental factors are known to affect human homosexual (HS) preference, sibling concordances and population patterns related to HS indicate that genetic components are also influencing this trait in humans. We argue that multilocus, partially Xlinked genetic factors undergoing sexually antagonistic selection that promote maternal female fecundity at the cost of occasional male offspring homosexuality are the best candidates capable of explaining the frequency, familial clustering, and pedigree asymmetries observed in HS male proband families. This establishes male HS as a paradigmatic example of sexual conflict in human biology. HS in females, on the other hand, is currently a more elusive phenomenon from both the empirical and theoretical standpoints because of its fluidity and marked environmental influence. Genetic and epigenetic mechanisms, the latter involving sexually antagonistic components, have been hypothesized for the propagation and maintenance of female HS in the population. However, further data are needed to truly clarify the evolutionary dynamics of this trait. Sexual conflict, the general theme of this collection, has emerged in the last decades as a main research topic in evolutionary biology. Its possible ubiquity and key role have become clear in many phenomena, from speciation to genetic diversity maintenance in populations, sexual phenotypic dimorphism, asymmetric mating and parenting strategies, antagonistic coevolution, and others (Bonduriansky and Chenoweth 2009;Rice et al. 2013; see also Gavrilets 2014). A most interesting example of sexual conflict is given by homosexual (HS) behavior and mate preference in humans, a topic whose societal impact is widely felt at present.Homosexuality is not confined just to our species, but is also occasionally present in numerous animals (Bagemihl 1999;Sommer and Vasey 2006), with permanent, long-term samesex pair bonding having been reported in some birds and ungulates (Bagemihl 1999;Ngun et al. 2011). The presence of not solely sporadic and opportunistic HS behavior has also been observed in nonhuman primates, which suggests our hominid ancestry might also have had HS individuals (Vasey 1995).The main evolutionary questions about HS in our species do not concern occasional HS behavior, which might have, in various con-

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“…Under this scenario, akin to the 'toxin-antidote' model, one might expect sex chromosomes to exhibit selfish behaviors to reduce the fitness of offspring that do not inherit them (e.g. X chromosomes harm male offspring whereas Y chromosomes harm female offspring), in what has been referred to as the 'sexually antagonistic zygotic drive' model (Friberg and Rice, 2015;Rice et al, 2008). Although there is tantalizing evidence in favor of this model (Friberg et al, 2011), its molecular basis is still unclear.…”

Section: Cytoplasmically Inherited Genomes: 'Mother's Curse'mentioning

confidence: 99%

Genetic conflicts: the usual suspects and beyond

McLaughlin

Malik

2017

Journal of Experimental Biology

144

127

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Selfishness is pervasive and manifests at all scales of biology, from societies, to individuals, to genetic elements within a genome. The relentless struggle to seek evolutionary advantages drives perpetual cycles of adaptation and counter-adaptation, commonly referred to as Red Queen interactions. In this review, we explore insights gleaned from molecular and genetic studies of such genetic conflicts, both extrinsic (between genomes) and intrinsic (within genomes or cells). We argue that many different characteristics of selfish genetic elements can be distilled into two types of advantages: an overreplication advantage (e.g. mobile genetic elements in genomes) and a transmission distortion advantage (e.g. meiotic drivers in populations). These two general categories may help classify disparate types of selfish genetic elements.

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Sexually Antagonistic Zygotic Drive: A New Form of Genetic Conflict between the Sex Chromosomes

Cited by 10 publications

References 28 publications

Sex‐specific allelic transmission bias suggests sexual conflict at MC1R

Sex‐specific allelic transmission bias suggests sexual conflict at MC1R

Human Homosexuality: A Paradigmatic Arena for Sexually Antagonistic Selection?

Genetic conflicts: the usual suspects and beyond

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