Academic journal article Genetics

Expansion of the Pseudo-Autosomal Region and Ongoing Recombination Suppression in the Silene Latifolia Sex Chromosomes

Academic journal article Genetics

Expansion of the Pseudo-Autosomal Region and Ongoing Recombination Suppression in the Silene Latifolia Sex Chromosomes

Article excerpt

ABSTRACT There are two very interesting aspects to the evolution of sex chromosomes: what happens after recombination between these chromosome pairs stops and why suppressed recombination evolves. The former question has been intensively studied in a diversity of organisms, but the latter has been studied largely theoretically. To obtain empirical data, we used codominant genie markers in genetic mapping of the dioecious plant Silene latifolia, together with comparative mapping of S. latifolia sex-linked genes in S. vulgaris (a related hermaphrodite species without sex chromosomes). We mapped 29 S. latifolia fully sex-linked genes (including 21 newly discovered from transcriptome sequencing), plus 6 genes in a recombining pseudo-autosomal region (PAR) whose genetic map length is ~25 cM in both male and female meiosis, suggesting that the PAR may contain many genes. Our comparative mapping shows that most fully sex-linked genes in S. latifolia are located on a single S. vulgaris linkage group and were probably inherited from a single autosome of an ancestor. However, unexpectedly, our maps suggest that the S. latifolia PAR region expanded through translocation events. Some genes in these regions still recombine in S. latifolia, but some genes from both addition events are now fully sex-linked. Recombination suppression is therefore still ongoing in S. latifolia, and multiple recombination suppression events have occurred in a timescale of few million years, much shorter than the timescale of formation of the most recent evolutionary strata of mammal and bird sex chromosomes.

AN important question concerning the evolution of sex chromosomes is why recombination suppression evolves between the evolving Y and X chromosomes, leading to subsequent genetic degeneration of Y chromosomes in XY chromosome pairs (and of the W in ZW pairs) and to accumulation of repetitive sequences and, ultimately, to heterochromatinization (e.g., Charlesworth and Charlesworth 2000; Charlesworth et al. 2005; Bachtrog 2006; Bergero and Charlesworth 2009). It is now understood that the large non-recombining regions of sex chromosomes in mammals have expanded over evolutionary time, forming "evolutionary strata" with differing levels of sequence divergence between X- and Y-gene pairs, from ancient highly diverged regions, to regions in which the genes started diverging much more recently, which are located closest to the pseudo-autosomal region (PAR) on the X chromosome genetic and physical maps (Lahn and Page 1999; Skaletsky et cd. 2003; Marais et al 2008). The more recent evolutionary strata were formed by recombination suppression in regions formed by an addition of autosomal genetic material to the sex chromosomes (Waters et ?ι. 2001), demonstrating that suppressed recombination spread from the ancestral sex chromosomal region into initially recombining regions. The PAR is shared across Eutherian mammals (despite differences in its boundary and the recent addition of a second PAR, PAR2, in humans), which is a physically small remnant of the added region, which is still autosomal in marsupials (Waters etc! 2001).

The major current explanation for the evolution of expanded nonrecombining regions of sex chromosomes is sexual antagonism. According to this theory, sexually antagonistic (SA) alleles that arise in sex chromosomes' recombining regions can be maintained polymorphically in populations because one allele benefits one sex, but harms the other (Jordan and Charlesworth 2012). Such a polymorphic situation selects for reduced recombination with the fully sex-linked (sex-determining) region, because this increases transmission of the male-benefit allele to males and reduces transmission of these alleles to females (Charlesworth and Charlesworth 1980; Rice 1987; Mank and Ellegren 2009; Jordan and Charlesworth 2012). However, alternatives exist [see Discussion in the accompanying article in this issue (Qiu et al. 2013)], and, no direct evidence currently connects SA alleles to the evolution of reduced recombination of Y or W sex chromosomes. …

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