Evans BJ et al. (2022), New insights into Xenopus sex chromosome genomi...

XB-ART-59303

J Evol Biol 2022 Dec 01;3512:1777-1790. doi: 10.1111/jeb.14078.

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New insights into Xenopus sex chromosome genomics from the Marsabit clawed frog X. borealis.

Evans BJ , Mudd AB , Bredeson JV , Furman BLS , Wasonga DV , Lyons JB , Harland RM , Rokhsar DS .

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In many groups, sex chromosomes change frequently but the drivers of their rapid evolution are varied and often poorly characterized. With an aim of further understanding sex chromosome turnover, we investigated the polymorphic sex chromosomes of the Marsabit clawed frog, Xenopus borealis, using genomic data and a new chromosome-scale genome assembly. We confirmed previous findings that 54.1 Mb of chromosome 8L is sex-linked in animals from east Kenya and a laboratory strain, but most (or all) of this region is not sex-linked in natural populations from west Kenya. Previous work suggests possible degeneration of the Z chromosomes in the east population because many sex-linked transcripts of this female heterogametic population have female-biased expression, and we therefore expected this chromosome to not be present in the west population. In contrast, our simulations support a model where most or all of the sex-linked portion of the Z chromosome from the east acquired autosomal segregation in the west, and where much genetic variation specific to the large sex-linked portion of the W chromosome from the east is not present in the west. These recent changes are consistent with the hot-potato model, wherein sex chromosome turnover is favoured by natural selection if it purges a (minimally) degenerate sex-specific sex chromosome, but counterintuitively suggest natural selection failed to purge a Z chromosome that has signs of more advanced and possibly more ancient regulatory degeneration. These findings highlight complex evolutionary dynamics of young, rapidly evolving Xenopus sex chromosomes and set the stage for mechanistic work aimed at pinpointing additional sex-determining genes in this group.

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Species referenced: Xenopus tropicalis Xenopus laevis Xenopus borealis
Genes referenced: dm-w dmrt1
GO keywords: sex chromosome [+]

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	FIGURE 1 Evolutionary scenarios (left) for the origin of geographically structured variation in X. borealis sex chromosomes. Red font indicates the population with the newest or most recent change in sex chromosomes. Simulations corresponding to these scenarios are depicted on the right, with further details provided in the main text and Supplement. θ refers to the population polymorphism parameter of the east (East) and west (West) populations, which are equal to 4Neμ, where Ne is the effective population size and μ is the mutation rate and τ0 and τ1 refer to divergence times in 4Ne generations.
	FIGURE 2 Using the new draft genome assembly for X. borealis and previously published RRGS data, we replicated the finding of sex linkage of the first 54.1 Mb of Chr8L, highlighted in red, in the east population (outer ring) and laboratory strain (central ring) (Furman & Evans, 2016, 2018) but not the west population (inner ring; Song et al., 2020). We additionally identify a spurious signal of sex linkage below 23 Mb on Chr7S in the east population, highlighted in blue. Colours of dots indicate the negative natural logarithm of the probability of association of genetic variation with sex as indicated in the legend. The sample sizes are five females and five males from east Kenya, 24 females and 22 males from the laboratory strain, and 16 females and 15 males from the west. S and L refer to X. borealis subgenomes (see Supplement). For the west population, similar results are recovered when RRGS data from four wild-caught females and four wild-caught males from Njoro (in central Kenya) are added.
	FIGURE 3 Pairwise nucleotide diversity of polymorphic sites in 2 Mb genomic windows of the sex-linked (<54.1 Mb, in red) and non-sex-linked (blue) portions of Chr8L in X. borealis from east Kenya based on RRGS data.Mb, in red) and non-sex-linked (blue) portions of Chr8L in X. borealis from east Kenya based on RRGS data. Genomic data were collected from the left-most female and left-most male.
	FIGURE 4 Contour plot of the natural log likelihoods of combinations of parameter settings for Scenarios 1&2 (left), Scenario 3a (center), and Scenario 3b (right). Model parameters (τ0, τ1) correspond to the time of population subdivision between the east and west, and recombination suppression between the W and Z chromosomes in the east population, as defined in Fig. 1. In all models, τ1 < τ0 (hence the triangular contour plots). The parameter combinations with the best fit to the observed data are warmer colors; parameter combinations with no accepted simulations are white; a white circle indicates the maximum likelihood parameter combination of the best fit model.
	Figure S1. RRGS genotypes on Chr8L from 10 X. borealis individuals from east Kenya (Wundyani) is consistent with recombination suppression between the W and Z chromosomes from 0–54.1 Mb. In this region, the five females have a much higher density of heterozygous positions (in gray) than the males. The x-axis is not to scale because it depends on the number of called genotypes. The higher densities of missing (white) genotypes are indicative of lower coverages for individuals BJE4516, BJE4541, and BJE4540.
	Fig. S2. Pairwise nucleotide diversity of polymorphic sites in 2 Mb genomic windows of the (pseudo-) sex-linked (<23.0 Mb, in red) and non-sex-linked portions of Chr7S in X. borealis from east Kenya based on RRGS data. Samples BJE4515 and BJE4536 were also used for WGS sequencing.
	Figure S3. RRGS genotypes on Chr7S from 10 X. borealis individuals from east Kenya (Wundyani) distinguishes two large haplotype blocks from 0-23 Mb. As indicated in the legend, homozygous genotypes for the reference allele are light blue, for the alternate allele are black, heterozygous genotypes are gray, and missing genotypes are white. Below 23 Mb, three males are homozygous for one haplotype block and two females are homozygous for the other (red and blue boxes); five individuals – two males, three females – are heterozygous for both haplotype blocks (dark gray box with many heterozygous sites). Individuals that are homozygous for these haplotype blocks have low diversity in this region (Fig. S2). The x-axis is not to scale because it depends on the number of called genotypes.
	Figure S4. Natural logarithm of the female/male polymorphism ratio for the pairs from the east (outer track), lab (center track), and west (inner track) in non-overlapping100kb genomic windows. Highlighted regions follow Fig. 2 and color is used to indicate ratio values as detailed in the legend (the natural logarithms of 2 and -2 are 0.69 and -0.69 respectively). Regions discussed in the text are highlighted in blue, red, and gray.
	Figure S5. Principal components analysis of the six WGS samples highlights variation in the lab strain. Analyses were performed separately for the portion of Chr8L that is sex-linked in the east and lab strain (<54.1 Mb, left) and the rest of the genome (right). The first and second eigenvectors captured 40.1% and 26.1% (left) and 39.3% and 26.5% (right) of genotypic variation. In the sex-linked region, the east and lab strain females cluster more closely together compared to the rest of the genome but with divergence attributable to variation in their W and Z chromosomes. In the non-sex-linked region, there is more variation between the lab strain individuals than between intra-population comparisons from the west or east.
	Figure S6. Count of SNPs per 100,000 base pair windows (y-axis) in genomic data from the west female (red) or west male (blue) that are heterozygous in each of these individuals and each female from the east and lab strain, but homozygous in the other west individual and each male from the east and lab strain in the portion of Chr8L that is sex-linked in the east and lab strain (x-axis). Red peaks are candidate regions containing a trigger for female sex determination among all X. borealis populations and the blue line establishes an expectation for this pattern in the absence of sex-linkage. Sanger sequencing of six labeled regions identified only sex-shared polymorphism with none fixed in females: mtm8 (12 females, 10 males); abcb7 (8 females, 5 males); region 1 (11 females, 10 males); region 2 (6 females, 3 males); nr5a1 (13 females, 10 males (Song et al., 2020), sox3 (29 females, 19 males (Song et al., 2020), which suggests none of these regions is sex-linked in the west.
	Fig. S7. Depths of coverage <54.1 and >54.1 Mb on Chr8L are similar in all individuals. Each dot represents the depth of one genomic position that is polymorphic in at least one of the six individuals with genomic data.
	Fig. S8. Depths of coverage <23.0 and >23.0 Mb on Chr7S are similar in all individuals. Each dot represents the depth of one genomic position that is polymorphic in at least one of the six individuals with genomic data.
	Fig. S9. Depth of coverage has low within individual variation by genomic region below 54.1 and above 54.1 Mb on Chr8L, which is inconsistent with the possibility of large-scale duplication or deletion in the sex-linked region. Lines for each individual is the rolling mean depth over 1,000 polymorphic positions.
	Fig. S10. Depth of coverage has low within individual variation by genomic region below 23.0 and above 23.0 Mb on Chr7S, which is also inconsistent with the possibility of large-scale duplication or deletion in the sex-linked region. Lines for each individual is the rolling mean depth over 1,000 polymorphic positions.

References [+] :

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