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Haploid selection, sex ratio bias, and transitions between sex-determining systems.

ABSTRACT: Sex determination is remarkably dynamic; many taxa display shifts in the location of sex-determining loci or the evolution of entirely new sex-determining systems. Predominant theories for why we observe such transitions generally conclude that novel sex-determining systems are favoured by selection if they equalise the sex ratio or increase linkage with a locus that experiences different selection in males versus females. We use population genetic models to extend these theories in two ways: (1) We consider the dynamics of loci very tightly linked to the ancestral sex-determining loci, e.g., within the nonrecombining region of the ancestral sex chromosomes. Variation at such loci can favour the spread of new sex-determining systems in which the heterogametic sex changes (XY to ZW or ZW to XY) and the new sex-determining region is less closely linked (or even unlinked) to the locus under selection. (2) We consider selection upon haploid genotypes either during gametic competition (e.g., pollen competition) or meiosis (i.e., nonmendelian segregation), which can cause the zygotic sex ratio to become biased. Haploid selection can drive transitions between sex-determining systems without requiring selection to act differently in diploid males versus females. With haploid selection, we find that transitions between male and female heterogamety can evolve so that linkage with the sex-determining locus is either strengthened or weakened. Furthermore, we find that sex ratio biases may increase or decrease with the spread of new sex chromosomes, which implies that transitions between sex-determining systems cannot be simply predicted by selection to equalise the sex ratio. In fact, under many conditions, we find that transitions in sex determination are favoured equally strongly in cases in which the sex ratio bias increases or decreases. Overall, our models predict that sex determination systems should be highly dynamic, particularly when haploid selection is present, consistent with the evolutionary lability of this trait in many taxa.

SUBMITTER: Scott MF

PROVIDER: S-EPMC6042799 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:To date, research on the evolution of sex chromosomes has focused on sexually antagonistic selection among diploids, which has been shown to be a potent driver of the strata and reduced recombination that characterize many sex chromosomes. However, significant selection can also occur on haploid genotypes during less conspicuous life cycle stages, e.g., competition among sperm/pollen or meiotic drive during gamete/spore production. These haploid selective processes are typically sex-specific, e.g., gametic/gametophytic competition typically occurs among sperm/pollen, and meiotic drive typically occurs during either spermatogenesis or oogenesis. We use models to investigate whether sex-specific selection on haploids could drive the evolution of recombination suppression on the sex chromosomes, as has been demonstrated for sex-specific selection among diploids. A potential complication is that zygotic sex-ratios become biased when haploid selected loci become linked to the sex-determining region because the zygotic sex ratio is determined by the relative number and fitness of X- vs. Y-bearing sperm. Despite causing biased zygotic sex-ratios, we find that a period of sex-specific haploid selection generally favors recombination suppression on the sex chromosomes. Suppressed recombination is favored because it allows associations to build up between haploid-beneficial alleles and the sex that experiences haploid selection most often (e.g., pollen beneficial alleles become strongly associated with the male determining region, Y or Z). Haploid selected loci can favor recombination suppression even in the absence of selective differences between male and female diploids. Overall, we expand our view of the sex-specific life cycle stages that can drive sex chromosome evolution to include gametic competition and meiotic drive. Based on our models, sex chromosomes should become enriched for genes that experience haploid selection, as is expected for genes that experience sexually antagonistic selection. Thus, we generate a number of predictions that can be evaluated in emerging sex chromosome systems.

Project description:ImportanceSex is a variable that is poorly controlled for in clinical research.ObjectivesTo determine if sex bias exists in human surgical clinical research, to determine if data are reported and analyzed using sex as an independent variable, and to identify specialties in which the greatest and least sex biases exist.Design, setting, and participantsFor this bibliometric analysis, data were abstracted from 1303 original peer-reviewed articles published from January 1, 2011, through December 31, 2012, in 5 surgery journals.Main outcomes and measuresStudy type, location, number and sex of participants, degree of sex matching of included participants, and inclusion of sex-based reporting, statistical analysis, and discussion of data.ResultsOf 2347 articles reviewed, 1668 (71.1%) included human participants. After excluding 365 articles, 1303 remained: 17 (1.3%) included males only, 41 (3.1%) included females only, 1020 (78.3%) included males and females, and 225 (17.3%) did not document the sex of the participants. Although female participants represent more than 50% (n = 57 688 606) of the total number (115 377 213) included, considerable variability existed with the number of male (46 111 818), female (58 805 665), and unspecified (10 459 730) participants included among the journals, between US domestic and international studies, and between single vs multicenter studies. For articles included in the study, 38.1% (497 of 1303) reported these data by sex, 33.2% (432 of 1303) analyzed these data by sex, and 22.9% (299 of 1303) included a discussion of sex-based results. Sex matching of the included participants in the research overall was poor, with 45.2% (589 of 1303) of the studies matching the inclusion of both sexes by 50%. During analysis of the different surgical specialties, a wide variation in sex-based inclusion, matching, and data reporting existed, with colorectal surgery having the best matching of male and female participants and cardiac surgery having the worst.Conclusions and relevanceSex bias exists in human surgical clinical research. Few studies included men and women equally, less than one-third performed data analysis by sex, and there was wide variation in inclusion and matching of the sexes among the specialties and the journals reviewed. Because clinical research is the foundation for evidence-based medicine, it is imperative that this disparity be addressed so that therapies benefit both sexes.

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Haploid selection, sex ratio bias, and transitions between sex-determining systems.

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