Haploid Selection Favors Suppressed Recombination Between Sex Chromosomes Despite Causing Biased Sex Ratios

Abstract

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.

Keywords: meiotic drive; pollen competition; recombination evolution; sex chromosomes; sex ratio; sperm competition.

Figure 1

XY and ZW diploid genetic sex determination systems. In our model, haploid selection occurs during gamete/gametophyte production (meiotic drive) and/or competition (gametic competition) in one sex. In this case, haploid selection occurs in males, as indicated by the dashed circle. In an XY system, male haploid selection causes the zygotic sex ratio to become biased when X- and Y-bearing gametes/gametophytes have different haploid fitnesses.

Figure 2

The zygotic sex ratio is biased by linkage between an XY SDR and a locus that experiences competition among male gametes. Here, we plot the zygotic sex ratio at equilibrium assuming that all individuals have the same recombination rate, r (fixed for modifier allele M). Male-biased sex ratios result when the Y becomes associated with alleles conferring high sperm fitness (solid line: $w_{Aa}=0.97,$ $w_{AA}=0.91,$ $w_a^{\mathrm{\text{♂}}}=0.9,$ $w_A^{\mathrm{\text{♂}}}=1,$ dashed line: $w_{Aa}=0.92,$ $w_{AA}=0.8,$ $w_a^{\mathrm{\text{♂}}}=1,$ $w_A^{\mathrm{\text{♂}}}=1.25,$ both with $w_{ij}^{\mathrm{\text{♂}}}=w_{ij}^{\mathrm{\text{♀}}}=w_{ij},$ $w_{aa}=1$ such that selection is ploidally antagonistic). Female-biased sex ratios can, however, arise if the haploid-beneficial allele is also strongly favored in females and becomes associated with the X (dotted line: $w_{aa}^{\mathrm{\text{♂}}}=1,$ $w_{Aa}^{\mathrm{\text{♂}}}=0.94,$ $w_{AA}^{\mathrm{\text{♂}}}=0.8,$ $w_{aa}^{\mathrm{\text{♀}}}=1,$ $w_{Aa}^{\mathrm{\text{♀}}}=1.14,$ $w_{AA}^{\mathrm{\text{♀}}}=1.2,$ $w_a^{\mathrm{\text{♂}}}=1,$ $w_A^{\mathrm{\text{♂}}}=1.1,$ such that selection in diploids is sexually antagonistic).

Figure 3

A modifier that reduces the recombination rate between the (A) locus and the SDR can spread to fixation despite causing sex ratios to become biased. We assume that the population initially has loose linkage between the (A) locus and the SDR ($r_{MM}=0.5,$ where M is initially fixed), and allow allele frequencies to reach a polymorphic equilibrium. We then introduce a modifier allele m that reduces the recombination rate between (A) locus and the SDR ($r_{Mm}=0.02,$ $r_{mm}=0.01$); in generation 0, m is at frequency 0.01 and in linkage equilibrium with M. In (A) the M locus lies between the (A) locus and the SDR (e.g., a fusion) with no crossover interference such that $\rho =\left(r_{Mm}-R^{\mathrm{\text{♂}}}\right)/\left(1-2R^{\mathrm{\text{♂}}}\right),$ where $R^{\mathrm{\text{♂}}}=R^{\mathrm{\text{♀}}}=\mathrm{0.005.}$ In (B), the M locus is autosomal and unlinked to either the SDR or (A) locus: $R^{\mathrm{\text{♂}}}=R^{\mathrm{\text{♀}}}=\rho =1/2.$ The autosomal recombination suppressor spreads more slowly (note change of x-axis scale), but it spreads despite an increasingly biased zygotic sex ratio. Fitness parameters are as in the solid curve in Figure 2. That is, selection is ploidally antagonistic with A favored during gametic competition (see Figure S3 in File S2 and Figure S4 in File S2 for meiotic drive). Curves show the frequencies of the recombination suppression mutant, m, among sperm (black curve), the A allele among Y-bearing sperm (green curve), the A allele among X-bearing sperm (purple curve), and male zygotes (dashed black curve, shown against the scale on the right hand side).

Figure A1

Selection can favor increased recombination between the SDR and a selected locus that is closely linked to the SDR ($r_{ij}\approx 0$), even when selection in males is not overdominant. The gray regions show where one or more of the polymorphic equilibria are stable, and thus recombination modifiers can affect fitness. Colored regions show where increased recombination is favored in a population at equilibrium $\left(A\right)$ in blue, $\left(B\right)$ in green, $\left(A^{\prime }\right)$ in red, and $\left(B^{\prime }\right)$ in orange. Since this model is symmetrical, red/orange regions can be exchanged with blue/green regions if the labeling of A and a alleles is switched. Across columns, we vary the fitness of a-bearing haploids relative to the A-bearing haploids ($w_A^{\mathrm{\text{♂}}}=1$). Gray lines show the fitness of heterozygous diploids $w_{Aa}^k=1.$ In the first row, there are no differences in selection between male and female diploids ($w_{ij}^{\mathrm{\text{♀}}}=w_{ij}^{\mathrm{\text{♂}}}=w_{ij}$), where $w_{aa}$ and $w_{AA}$ are varied along the x and y axes, respectively. As haploid selection becomes stronger, increased recombination can evolve with weaker overdominance in diploids, and also with ploidally antagonistic selection ($w_{aa}>1>w_{AA}$). In the second and third rows, we consider sex differences in selection, where $w_{aa}^{\mathrm{\text{♂}}}$ and $w_{AA}^{\mathrm{\text{♂}}}$ are varied along the x and y axes ($w_{Aa}^{\mathrm{\text{♂}}}=1$). In the second row, where selection in females is overdominant ($w_{AA}^{\mathrm{\text{♀}}}=0.75,$ $w_{Aa}^{\mathrm{\text{♀}}}=1,$ $w_{aa}^{\mathrm{\text{♀}}}=0.75$), increased recombination can be favored when selection is directional (or underdominant) in males, and haploid selection is moderately strong. In the third row, selection favors the A allele in females ($w_{AA}^{\mathrm{\text{♀}}}=1.05,$ $w_{Aa}^{\mathrm{\text{♀}}}=1,$ $w_{aa}^{\mathrm{\text{♀}}}=0.75$) and increased recombination can be favored with overdominance in males or sexually antagonistic selection ($w_{AA}^{\mathrm{\text{♂}}}<1<w_{aa}^{\mathrm{\text{♂}}}$). For this plot, we assume that the modifier of recombination is unlinked ($R^{\mathrm{\text{♀}}}=R^{\mathrm{\text{♂}}}=1/2$).