Reply to Wright et al.: How to explain the absence of extensive Y-specific regions in the guppy sex chromosomes

Wright et al. (1) are correct that our genomic data for the guppy sex chromosome are not dissimilar from theirs. However, our conclusion truly differs from their previous chief conclusion that “evolutionary strata” are evolving (2). Strata are sex chromosome regions that evolved suppressed recombination in separate events, each establishing a nonrecombining region, isolating Y-linked sequences from their X-linked alleles for substantial evolutionary times and creating physical regions of an X/Y or Z/W sex chromosome pair with different divergence. Sequence divergence suggests that the most recent recombination suppression event in humans occurred at least 30 million years ago (3, 4), and more recently in plant sex chromosomes (5–7). In contrast, both guppy genomic datasets (2, 8) are compatible with some recombination occurring across much of the X/Y pair.

Using genetic mapping, we show that recombination events outside the pseudoautosomal region, and beyond the maleness factor, do occur, albeit rarely (8). These events, together with crossovers in female meiosis, will prevent the evolution of diverged Y male-specific regions and formation of evolutionary strata (Fig. 1). Wright et al. (1) also acknowledge that even very rare recombination will prevent isolation of Y- from X-linked sequences but claim that the occurrence of such centromere-proximal crossover events in male meiosis might differ between populations. However, our results show that such recombination events in male meiosis are rare in both low- and high-predation populations, and the high-predation males do not show crossovers in the region where younger strata are claimed to have not yet evolved (8). Therefore, any difference in recombination rates in the centromere-proximal region must be very small, and the existence of evolutionary strata is not supported.

Fig. 1.

Breakdown of X-Y differentiation during male and female meiosis in guppy sex chromosomes. (Top) Chromosome pair in a male; blue indicates the chromosome carrying the male-determining (maleness) factor. (Middle) A crossover in male meiosis just to the left of the male-determining factor generates a recombinant genotype without the maleness factor. This can enter the female population and recombine further with an X chromosome (shown in red) to produce genotypes shared by both male and female populations. (Bottom) Recombinants produced in female meiosis can reacquire the maleness factor by further recombination events after reentering the male population.

Concerning the read mapping, Wright et al. (2) used male/female coverage differences to infer that sequences have diverged, requiring stringent mapping to ensure that sequence reads containing even a single male-specific variant were excluded. This method can indeed detect regions with X-Y sequence divergence, which will have lower coverage in males than females. We, however, quantified differentiation of X and Y sequences using F_ST, which can reveal X-Y differentiation in nonrecombining regions, if present (8). Our mapping rates to the reference genome, and coverage in our sample of 10 males and 6 females, were high enough to detect variants accurately (8). We found extremely few sequence variants with genotypes compatible with complete sex linkage. Importantly, these were not concentrated in the sex-determining region and cannot correspond to the claimed old evolutionary stratum. Most likely, the differentiation evidenced in both genomic datasets represents linkage disequilibrium within a genome region undergoing very rare recombination, not strata resulting from an extended evolutionary history involving multiple recombination suppression events.

The loss of most Y-linked genes in the closely related species Poecilia picta supports the view that the guppy Y chromosome is young. “Turnover events,” creating young sex-chromosome systems, are observed in several fish (9, 10) and other organisms (11) and often allow continued recombination, producing sex-determining regions without evolutionary strata.