Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2014 Jun;197(2):531-41.
doi: 10.1534/genetics.113.156026. Epub 2014 Feb 27.

Signatures of sex-antagonistic selection on recombining sex chromosomes

Mark Kirkpatrick  1 , Rafael F Guerrero  2
Affiliations

Signatures of sex-antagonistic selection on recombining sex chromosomes

Mark Kirkpatrick et al. Genetics. 2014 Jun.

Abstract

Sex-antagonistic (SA) selection has major evolutionary consequences: it can drive genomic change, constrain adaptation, and maintain genetic variation for fitness. The recombining (or pseudoautosomal) regions of sex chromosomes are a promising setting in which to study SA selection because they tend to accumulate SA polymorphisms and because recombination allows us to deploy the tools of molecular evolution to locate targets of SA selection and quantify evolutionary forces. Here we use coalescent models to characterize the patterns of polymorphism expected within and divergence between recombining X and Y (or Z and W) sex chromosomes. SA selection generates peaks of divergence between X and Y that can extend substantial distances away from the targets of selection. Linkage disequilibrium between neutral sites is also inflated. We show how the pattern of divergence is altered when the SA polymorphism or the sex-determining region was recently established. We use data from the flowering plant Silene latifolia to illustrate how the strength of SA selection might be quantified using molecular data from recombining sex chromosomes.

Keywords: coalescent; genetics of sex; model; neutral polymorphism; sex chromosome.

PubMed Disclaimer

Figures

Figure 1
Figure 1
Expected coalescence times between pairs of genes sampled from X and Y chromosomes. Left and center, the regions flanking the SDR; right, the region surrounding locus A. Solid curves show the analytic results when SA selection acts on locus A (shown by the vertical line in the right panel). Shaded curves are the corresponding cases with no SA polymorphism. Circles are simulation results. The frequencies of allele A1 on X and Y chromosomes are x = 0.845 and y = 0.155.
Figure 2
Figure 2
Expected divergence with sex-antagonistic selection on a site at ρ = 100. Top, FST between X and Y chromosomes; bottom, FST between sex chromosomes sampled from males and females. The frequencies of allele A1 on X and Y chromosomes (that is, x and y) are case 1 = (0.618, 0.381), case 2 = (0.845, 0.155), and case 3 = (0.912, 0.082).
Figure 3
Figure 3
Expected divergence between genes sampled from X and Y chromosomes in the vicinity of a locus under sex-antagonistic selection that is weakly linked to the SDR. The SA locus is at ρ=0, and the SDR lies far to the left (at ρ=−1000). Solid curves, the full model; lines with light shading, the linearized weak linkage approximation (Equation 4); horizontal bars with dark shading, the region of high FST defined by Equation 5. The parameter values for the three panels correspond to cases 1, 2, and 3 in Figure 2 but with ρSA = 1000. Note the differences in the vertical scales of the panels.
Figure 4
Figure 4
Divergence between X and Y chromosomes at the sex-antagonistic locus A plotted against the strength of sex-antagonistic selection (measured relative to the recombination rate between locus A and the SDR).
Figure 5
Figure 5
The correlation in coalescence times, R, between pairs of neutral sites near a balanced polymorphism. Above the diagonal are results for simple balancing selection on an autosome; below the diagonal are results for the sex-antagonistic case. Parameters are those for case 2 in Figure 2. The black circle shows the selected locus, and the dashed box shows the region of elevated linkage disequilibrium.
Figure 6
Figure 6
Expected coalescence times and divergence between X and Y chromosomes following establishment of a new male-determining gene on an autosome (left) or new SA polymorphism at locus A (right). Solid curves show results for establishment events 20N generations ago and shaded curves show results for events 0.2N generations ago. Other parameters are as in case 2 of Figure 1. Circles are values from simulations (lines are added for clarity). Left, following the establishment of a neo-Y on the chromosome carrying locus A; right, following the establishment of a new sex-antagonistic polymorphism at locus A on an old sex chromosome. Top, dashed curves are for a pair of genes sampled from X and Y chromosomes and solid curves are when both genes are from X chromosomes.
See this image and copyright information in PMC

References

    1. Arnqvist G., Rowe L., 2005. Sexual Conflict. Princeton University Press, Princeton, NJ.
    1. Bachtrog D., 2006. A dynamic view of sex chromosome evolution. Curr. Opin. Genet. Dev. 16: 578–585 - PubMed
    1. Bachtrog D., Kirkpatrick M., Mank J. E., McDaniel S. F., Pires J. C., et al. , 2011. Are all sex chromosomes created equal? Trends Genet. 27: 350–357 - PubMed
    1. Barton N., Bengtsson B. O., 1986. The barrier to genetic exchange between hybridizing populations. Heredity 57: 357–376 - PubMed
    1. Beaumont M. A., 2010. Approximate Bayesian computation in evolution and ecology, Annu. Rev. Ecol. Evol. Syst. 41: 379–406

Publication types