Transitions between male and female heterogamety caused by sex-antagonistic selection - PubMed (original) (raw)
Transitions between male and female heterogamety caused by sex-antagonistic selection
G Sander van Doorn et al. Genetics. 2010 Oct.
Abstract
Many animal taxa show frequent and rapid transitions between male heterogamety (XY) and female heterogamety (ZW). We develop a model showing how these transitions can be driven by sex-antagonistic selection. Sex-antagonistic selection acting on loci linked to a new sex-determination mutation can cause it to invade, but when acting on loci linked to the ancestral sex-determination gene will inhibit an invasion. The strengths of the consequent indirect selection on the old and new sex-determination loci are mediated by the strengths of sex-antagonistic selection, linkage between the sex-antagonistic and sex-determination genes, and the amount of genetic variation. Sex-antagonistic loci that are tightly linked to a sex-determining gene have a vastly stronger influence on the balance of selection than more distant loci. As a result, changes in linkage, caused, for example, by an inversion that captures a sex-determination mutation and a gene under sex-antagonistic selection, can trigger transitions between XY and ZW systems. Sex-antagonistic alleles can become more strongly associated with pleiotropically dominant sex-determining factors, which may help to explain biases in the rates of transitions between male and female heterogamety. Deleterious recessive mutations completely linked to the ancestral Y chromosome can prevent invasion of a neo-W chromosome or result in a stable equilibrium at which XY and ZW systems segregate simultaneously at two linkage groups.
Figures
Figure 1.—
A homologous transition from male to female heterogamety. (A) A feminizing allele segregating at a novel sex-determination locus on the ancestral sex chromosomes increases in frequency (solid circles) if it is more tightly linked to a sex-antagonistic locus than the ancestral master sex-determining gene ( and in this simulation). The spread of the novel W allele is accompanied by an increase in the frequency of the ancestral masculinizing Y allele in both male and female gametes (open and solid squares, respectively) and slight changes in the allele frequencies at the sex-antagonistic locus (open and solid triangles/dashed lines). (B) The homologous heterogamety transition is driven by sex-antagonistic selection, which acts indirectly on the sex-determination loci through their nonrandom genetic association with sex-antagonistic alleles. (C) Initially, the W allele spreads at a nearly constant exponential rate and simulated frequencies (solid circles) fall along a straight line when plotted on a logarithmic scale. Analytical expressions for the invasion fitness of the W allele (dashed line, loose-linkage result; solid line, tight-linkage result) predict the slope of this line (i.e., the exponential rate of increase) during the initial phase of the simulations. Fitness values for the genotypes 00, 01, and 11 in females were given by , , and , respectively, with and . Analogous expressions define fitness in males, with and . Mutations between sex-antagonistic alleles occurred at rate .
Figure 2.—
Validity of the analytical approximations. A homologous transition is modeled with a fixed distance between the ancestral and novel sex-determining loci (the rate of recombination between these loci is ), while the position of the sex-antagonistic locus (parameters: , , , , and ) is varied (horizontal axis). The vertical axis gives the invasion fitness of the W allele on the basis of numerical iterations of the exact population-genetic recursions of the model (solid circles), the tight-linkage approximation (solid curve), and the loose-linkage approximation (dashed curve). The latter performs well as long as recombination is a stronger force than selection (), while the tight-linkage approximation is accurate over the entire range of recombination rates (noticeable differences with the simulation results appear only when linkage between the sex-determination loci is very tight). We assumed H
aldane
's (1919) mapping function.
Figure 3.—
Heterogamety transitions are governed by a small subset of the sex-antagonistic genes. The invasion fitness of the W allele was calculated for 300,000 random genetic systems, each with 200 sex-antagonistic loci. In each simulation the sex-antagonistic loci were distributed over two linkage groups; two-thirds of the loci were randomly positioned on the ancestral sex chromosomes and the remaining one-third of the loci were randomly positioned on an autosome pair with the novel sex-determination gene. The size of both linkage groups was 100 cM. Despite the twofold bias favoring the ancestral sex-determination system and the large number of loci, we observed positive values of the invasion fitness in ∼10% of the cases. The right tail of the observed distribution of fitness values is shown, with dots indicating invasion fitness estimates from individual simulations (shaded dots, loose-linkage approximation; solid dots, tight-linkage approximation). In both cases, the right-tail behavior is well approximated by the fitness contribution of the single sex-antagonistic locus that is most tightly linked to the novel sex-determination gene (thin solid lines), indicating that the sex-antagonistic variation responsible for transitions between sex-determination systems may segregate at a very small subset of the sex-antagonistic loci. The selection coefficients for individual loci were drawn from a bivariate normal distribution with mean (0, 0) and a covariance matrix with common variance and correlation coefficient −0.8. The dominance coefficients were also drawn from a bivariate normal distribution [mean (0.5, 0.5), common variance , and correlation coefficient 0.7] with the additional constraint 0 ≤ h ≤ 1.
Figure 4.—
Protected polymorphism of two sex-determination factors on different linkage groups. Recessive deleterious alleles on the ancestral y chromosome can prevent the W allele from spreading to fixation, leading to a permanent state of multifactorial sex determination (equilibrium frequencies indicated by the dashed lines) if the deleterious alleles have fixed on the y chromosome and recombination with the x has been fully repressed. Even a tiny amount of recombination ( here), however, introduces genetic variation on the y chromosome and purges its deleterious alleles. When this happens, W ultimately fixes and the ancestral XY system is lost. In this simulation, a locus segregating for deleterious alleles (parameters: , , , and deleterious mutation rate ; allele frequencies in male and female gametes are shown by dotted lines with open and solid triangles, respectively) is linked to Y and an autosomal sex-antagonistic locus (parameters: , , , , , and ; allele frequencies are not shown) is linked to W.
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