Patterns and mechanisms of evolutionary transitions between genetic sex-determining systems

Abstract

The diversity and patchy phylogenetic distribution of genetic sex-determining mechanisms observed in some taxa is thought to have arisen by the addition, modification, or replacement of regulators at the upstream end of the sex-determining pathway. Here, I review the various evolutionary forces acting on upstream regulators of sexual development that can cause transitions between sex-determining systems. These include sex-ratio selection and pleiotropic benefits, as well as indirect selection mechanisms involving sex-linked sexually antagonistic loci or recessive deleterious mutations. Most of the current theory concentrates on the population-genetic aspects of sex-determination transitions, using models that do not reflect the developmental mechanisms involved in sex determination. However, the increasing availability of molecular data creates opportunities for the development of mechanistic models that can clarify how selection and developmental architecture interact to direct the evolution of sex-determination genes.

Figure 1.

Neutral and adaptive models of a transition from male to female heterogamety. The two panels illustrate the change of the gamete frequencies of the ancestral (horizontal axes) and novel (vertical axes) sex-determining alleles during a transition from XX♀/XY♂ GSD (male heterogamety) to ZZ♂/ZW♀ GSD (female heterogamety). For each panel, genetic assumptions are illustrated by means of schematic representations of the ancestral sex chromosome pair (gray) with the sex-determining locus, and a pair of autosomes (white) carrying a sex-determination mutation (A,B) and a sexually antagonistic locus (B only). (A) Invasion of an autosomal, epistatically dominant feminizing mutation W. In the absence of intrinsic fitness differences between sex-determination genotypes, the allele W can drift to fixation as the population moves stochastically along a line of equilibria (thick gray line) (Bull and Charnov 1977), away from the ancestral state in the lower left corner of the diagram. By the time variation at the ancestral sex-determining locus is lost and the allele W reaches fixation (in the upper right corner of genotype space), the former X chromosome has disappeared from the population. Populations initialized with arbitrary combinations of allele frequencies quickly evolve toward the line of equilibria (thin gray trajectories), under the influence of selection for a balanced sex ratio. The process of drift along the line of equilibria is illustrated by the results from a stochastic, individual-based implementation of the population-genetic model (black trajectory with open circles; gamete frequencies are plotted every 50 generations for a population of 1000 individuals). (B) A sexually antagonistic gene located on the same autosome pair as the feminizing mutation causes the W allele to spread as a result of indirect selection, supported by the development of linkage disequilibrium between W and the female beneficial allele B (van Doorn and Kirkpatrick 2010). A simulation of a large population of 1 · 10⁶ individuals illustrates the slow deterministic movement of the allele frequencies along a nearly neutral path close to the former line of equilibria (thick grey line). Small insets in A and B present a close-up view of evolutionary trajectories in the vicinity of the line of equilibria, confirming that movement along the line is no longer neutral in B.

Figure 2.

Contributions of linkage and sex-differential selection to sex-determination transitions. If selection is weak relative to the force of recombination, the effect of a sexually antagonistic locus on the fitness of a sex-determining mutation (measured as its exponential rate of spread, λ) is quantified by the expression (1) irrespective of many details of the ancestral sex-determining mechanism (van Doorn and Kirkpatrick 2007, 2010). Here, G_intra is the intrasexual additive genetic variance for fitness at the sexually antagonistic locus and G_inter is the corresponding genetic covariance between fitness in males and females. The parameters r and r′ denote the rates of recombination between the sexually antagonistic gene and the ancestral/novel sex-determining locus, respectively. (A) Equation 1 diverges when one of the recombination rates approaches zero, indicating that the direction of sex-determination transitions is strongly affected by patterns of linkage. This is illustrated for the fitness effect of a sexually antagonistic gene on an epistatically dominant feminizing mutation W that has originated on an ancestral XY sex chromosome pair. The fitness of the W-allele varies depending on the chromosomal position of the sexually antagonistic locus (horizontal axis). The strength of indirect selection is highest when the sexually antagonistic gene is tightly linked to either the novel or the ancestral sex-determining locus (the rate of recombination between the sex-determination genes was kept fixed at 0.08). The prediction based on Equation 1 (solid line) agrees with the results of simulations based on the exact population-genetic recursions (closed circles), except when linkage is tight. Various refinements of Equation 1 can be developed to resolve this problem (van Doorn and Kirkpatrick 2010), but these depend on details of the GSD system. (B) Equation 1 also indicates that transitions in the sex-determination system can occur under conditions that are more general than those typically considered in discussions of sexually antagonistic selection. It suffices for the relative fitness effects of the selected locus to be different in males and females; it is not necessary that the allele favored in males is detrimental to females (or vice versa). The latter condition is stricter, as it implies that the intersexual covariance in fitness G_inter has to be negative, whereas indirect selection on the sex-determination locus is already generated if the intersexual covariance is positive but smaller than G_intra. Therefore, also transiently polymorphic loci and deleterious alleles maintained by migration or mutation-selection balance contribute to the indirect selection force on sex-determination loci if they have different (but not necessarily antagonistic) fitness effects in males and females. This effect is illustrated for a locus on the ancestral sex chromosomes that carries recessive deleterious alleles (m). The deleterious alleles are assumed to be expressed only in females, such that the mutation initially can accumulate freely on the Y chromosome. The invasion of an autosomal, epistatically dominant feminizing allele W gives rise to a subpopulation of homozygous YY females in which the deleterious alleles are expressed, reducing the fitness of the W allele. The figure shows the magnitude of this fitness reduction as a function of the rate of recombination between the locus with deleterious alleles and the ancestral sex-determination locus. The prediction based on Equation 1 (solid line) matches again with the result of simulations (closed circles) except for very low recombination rates.