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Assessment of phylogenetic approaches to study the timing of recombination cessation on sex chromosomes.

ABSTRACT: The evolution of sex chromosomes is hypothesized to be punctuated by consecutive recombination cessation events, forming "evolutionary strata" that ceased to recombine at different time points. The demarcation of evolutionary strata is often assessed by estimates of the timing of recombination cessation (t_RC ) along the sex chromosomes, commonly inferred from the level of synonymous divergence or with species phylogenies at gametologous (X-Y or Z-W) sequence data. However, drift and selection affect sequences unpredictably and introduce uncertainty when inferring t_RC . Here, we assess two alternative phylogenetic approaches to estimate t_RC ; (i) the expected likelihood weight (ELW) approach that finds the most likely topology among a set of hypothetical topologies and (ii) the BEAST approach that estimates t_RC with specified calibration priors on a reference species topology. By using Z and W gametologs of an old and a young evolutionary stratum on the neo-sex chromosome of Sylvioidea songbirds, we show that the ELW and BEAST approaches yield similar t_RC estimates, and that both outperform two frequently applied approaches utilizing synonymous substitution rates (dS) and maximum likelihood (ML) trees, respectively. Moreover, we demonstrate that both ELW and BEAST provide more precise t_RC estimates when sequences of multiple species are included in the analyses.

SUBMITTER: Zhang H

PROVIDER: S-EPMC10086819 | biostudies-literature | 2022 Dec

REPOSITORIES: biostudies-literature

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Assessment of phylogenetic approaches to study the timing of recombination cessation on sex chromosomes.

Zhang Hongkai H Sigeman Hanna H Hansson Bengt B

Journal of evolutionary biology 20220727 12

The evolution of sex chromosomes is hypothesized to be punctuated by consecutive recombination cessation events, forming "evolutionary strata" that ceased to recombine at different time points. The demarcation of evolutionary strata is often assessed by estimates of the timing of recombination cessation (t<sub>RC</sub> ) along the sex chromosomes, commonly inferred from the level of synonymous divergence or with species phylogenies at gametologous (X-Y or Z-W) sequence data. However, drift and s ...[more]

PMID: 35895083

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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.

Dataset Information

Assessment of phylogenetic approaches to study the timing of recombination cessation on sex chromosomes.

Publications

Assessment of phylogenetic approaches to study the timing of recombination cessation on sex chromosomes.

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