Furman BLS and Evans BJ (2018), Divergent Evolutionary Trajectories of Two Youn...

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Genome Biol Evol 2018 Mar 01;103:742-755. doi: 10.1093/gbe/evy045.

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

Furman BLS, Evans BJ.

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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.

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Species referenced: Xenopus tropicalis Xenopus laevis Xenopus borealis
Genes referenced: dm-w

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	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).
	FIG. S1.—Using sex-specific linkage maps that were generated from sets of either female or male heterozygous sites, we determined (a) parental haplotypes. (b) A haplotype from each parent could either be inherited entirely (if no recombination happened in the genotyped region), or recombined. (c) Scoring offspring haplotypes for sex specific maps of each chromosome allows for visualization and counting of the number of recombination events and identification of genotyping errors or improbable double recombination events.
	FIG. S2.—SNPs from the X. borealis family heterozygous in the mother mapped to the genome of X. laevis. Sex-linkage is calculated following Goudet et al. (1996), followed by an FDR correction to account for multiple testing (significant genotypes are indicated by black dots). The gray lines in each plot represent the significance threshold of 0.05. The sex-linked marker on chr5S can be mapped to chromosome 8S and 8L when a larger amount of sequence data is used (see Results).
	FIG. S3.—Phased parental haplotypes in X. borealis offspring for the maternal (left column) and paternal (right column) linkage groups of chromosome 8L. In the maternal haplotypes, the beginning of chromosome 8L is completely linked to sex (all daughters with the same haplotype, 0, and all sons had haplotype 1), apart from two recombination events near the end. Note, this linkage map only spans the sex- linked region (see Methods). For the paternal map, haplotypes are evenly shared between the sexes, indicating non-sex-linked inheritance of the paternal Z chromosome. In the region of the paternal Z chromosomes that is homologous to the sex-linked region of the maternal sex chromosomes, several recombination events are observed.
	FIG. S4.—Median depth (DP) and genotype quality (GQ) for offspring of the X. borealis and X. laevis families for maternal heterozygous sites used in the sex linkage analysis of Fig. 1.
	FIG. S5.—SNPs from the X.laevis family heterozygous in the mother mapped to the genome of X.laevis. Sex-linkage is calculated following Goudet et al. (1996), followed by an FDR correction to account for multiple testing (significant at 0.05 colored black). The gray lines in each plot represent the significance threshold of 0.05.

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Adolfsson, Lack of dosage compensation accompanies the arrested stage of sex chromosome evolution in ostriches. 2013, Pubmed