Abstract
Classical models suggest that recombination rates on sex chromosomes evolve in a stepwise manner to localize sexually antagonistic variants in the sex in which they are beneficial, thereby lowering rates of recombination between X and Y chromosomes. However, it is also possible that sex chromosome formation occurs in regions with preexisting recombination suppression. To evaluate these possibilities, we constructed linkage maps and a chromosome-scale genome assembly for the dioecious plant Rumex hastatulus. This species has a polymorphic karyotype with a young neo-sex chromosome, resulting from a Robertsonian fusion between the X chromosome and an autosome, in part of its geographic range. We identified the shared and neo-sex chromosomes using comparative genetic maps of the two cytotypes. We found that sex-linked regions of both the ancestral and the neo-sex chromosomes are embedded in large regions of low recombination. Furthermore, our comparison of the recombination landscape of the neo-sex chromosome to its autosomal homolog indicates that low recombination rates mainly preceded sex linkage. These patterns are not unique to the sex chromosomes; all chromosomes were characterized by massive regions of suppressed recombination spanning most of each chromosome. This represents an extreme case of the periphery-biased recombination seen in other systems with large chromosomes. Across all chromosomes, gene and repetitive sequence density correlated with recombination rate, with patterns of variation differing by repetitive element type. Our findings suggest that ancestrally low rates of recombination may facilitate the formation and subsequent evolution of heteromorphic sex chromosomes.
Highlights
Summary chromosome formation occurs in regions with pre-existing recombination suppression
Sex chromosomes are valuable for the study of recombination evolution because they represent an example of convergent recombination suppression, and evolutionary theory predicts an important role for natural selection in this process
The major finding of this study is that the sex-linked regions of both cytotypes of R. hastatulus are embedded in a region of highly suppressed recombination which cannot be explained by a lack of X-Y recombination
Summary
Summary chromosome formation occurs in regions with pre-existing recombination suppression. Because of differences between the sexes in their optimal reproductive strategies [15], some alleles beneficial in one sex can be detrimental in the other sex and create a selective load in the population [14, 16] The cost of this genetic load can be resolved by the evolution of sex-specific gene expression [17], or by the invasion of recombination modifiers that link the sexually antagonistic variant with the genomic region responsible for determination of the sex to which that variant is beneficial [18]. Plant sex chromosomes are generally in earlier stages of divergence than the vertebrate sex chromosomes that led to the development of this “strata” model [26] and are especially useful for identifying the earliest stages of recombination evolution across sex chromosomes
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