Divergent Evolutionary Trajectories of Two Young, Homomorphic, and Closely Related Sex Chromosome Systems

Abstract

There exists extraordinary variation among species in the degree and nature of sex chromosome divergence. However, much of our knowledge about sex chromosomes is based on comparisons between deeply diverged species with different ancestral sex chromosomes, making it difficult to establish how fast and why sex chromosomes acquire variable levels of divergence. To address this problem, we studied sex chromosome evolution in two species of African clawed frog (Xenopus), both of whom acquired novel systems for sex determination from a recent common ancestor, and both of whom have female (ZW/ZZ) heterogamy. Derived sex chromosomes of one species, X. laevis, have a small region of suppressed recombination that surrounds the sex determining locus, and have remained this way for millions of years. In the other species, X. borealis, a younger sex chromosome system exists on a different pair of chromosomes, but the region of suppressed recombination surrounding an unidentified sex determining gene is vast, spanning almost half of the sex chromosomes. Differences between these sex chromosome systems are also apparent in the extent of nucleotide divergence between the sex chromosomes carried by females. Our analyses also indicate that in autosomes of both of these species, recombination during oogenesis occurs more frequently and in different genomic locations than during spermatogenesis. These results demonstrate that new sex chromosomes can assume radically different evolutionary trajectories, with far-reaching genomic consequences. They also suggest that in some instances the origin of new triggers for sex determination may be coupled with rapid evolution sex chromosomes, including recombination suppression of large genomic regions.

Fig. 1.

—Sex-linkage of SNPs on sex chromosomes of X. borealis and X. laevis. In each graph, the x-axis is the position on the sex chromosome using the coordinates of the X. laevis reference genome and the y-axis is the major daughter genotype frequency in sons and daughters (see Materials and Methods for details) with colors as defined in the key indicating whether or not a SNP is significantly associated with sex (FDR corrected P < 0.05). For each species, a diagram of a chromosome is shaded darker in the region of suppressed recombination. The inset phylogeny is from Furman and Evans (2016); DM-W is carried by female X. clivii, but its presence on chr2L has not been confirmed.

Fig. 2.

—Linkage map length (in cM) is positively correlated with the number of bp spanned by the map (based on the X. laevis genome) for maternal but not paternal linkage maps. Black “sex chr” dots indicate the linkage map of the sex chromosome of each species (chromosome 8 L in X. borealis, chromosome 2 L in X. laevis). Lines reflect linear model relationships; gray shading indicates the 95% confidence interval of this relationship. Additionally, chromosome 8S is highlighted for X. borealis, because it is the homeolog of the sex chromosome 8 L (see Results for details).

Fig. 3.

—Density plots of recombination events with respect to the relative position along chromosomes (chromosome length scaled to be between 0 and 1) in the maternal and paternal linkage maps of X. borealis and X. laevis.

Fig. 4.

—Nucleotide diversity (π) in X. borealis based on WGS data mapped to the X. laevis reference genome. (a) Median π by chromosome as measured in the six genomic categories; error bars indicate 95% CI bootstrap estimates (for further information on differences see supplementary S1.4, Supplementary Material online). The 8 L_NL category refers to the diversity measured on chromosome 8 L in the nonsex-linked region (57–120 Mb). (b) Box and whisker plot of π across six genomic categories (described in Materials and Methods); the y-axis is truncated at 0.05 for clarity. (c) Standardized nucleotide diversity of the female divided by the standardized nucleotide diversity of male in 1-Mb windows across chr8L; the completely sex-linked region is highlighted in dark purple, and the significantly sex linked region with suppressed recombination in light purple (see fig. 1).