W chromosome expression responds to female-specific selection

Moghadam, Hooman K.; Pointer, Marie A.; Wright, Alison E.; Berlin, Sofia; Mank, Judith E.

doi:10.1073/pnas.1202721109

Cited by 98 publications

(135 citation statements)

References 46 publications

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“…It thus appears that multiple losses of recombination have happened within an evolutionary time much shorter than that since the most recent strata were established in the sex chromosome systems of mammals (see Introduction) and birds (Lawson-Handley et al 2004;Nam and Ellegren 2008;Moghadam et al 2012). The most recent mammal stratum (5) is estimated to have formed 30 MYA, 5 MY before the divergence of the human and Old World monkey lineages (Hughes et al 2012), and stratum 4 10 MY earlier (Ross et al 2005), after PAR boundary shifts earlier in Eutherian mammal evolution (Van Laere et al 2008;Das et al 2009).…”

Section: Figurementioning

confidence: 99%

Expansion of the Pseudo-autosomal Region and Ongoing Recombination Suppression in the Silene latifolia Sex Chromosomes

Bergero

Qiu

Forrest³

et al. 2013

Genetics

122

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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 genic 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. It is now understood that the large nonrecombining 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 al. 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 al. 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 et al. 2001).The major current explanation for the evolution of expanded nonrecombining regions of sex chromosomes is

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Section: Figurementioning

confidence: 99%

Expansion of the Pseudo-autosomal Region and Ongoing Recombination Suppression in the Silene latifolia Sex Chromosomes

Bergero

Qiu

Forrest³

et al. 2013

Genetics

122

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“…On the chimpanzee and human Y chromosomes, there are only 40-80 intact genes, as compared to 1,098 protein-coding genes on the X chromosome. 26 expressed genes have been attributed to the chicken W chromosome 39 , whereas the Z chromosome has about 1,000 genes 40 , as in tongue sole. This observation points to a relatively recent evolutionary origin for the tongue sole sex chromosome pair, where degeneration on the W chromosome has not progressed to a stage at which almost its entire original gene content has disappeared.…”

Section: Genomic Organization and Evolution Of Z And Wmentioning

confidence: 99%

Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle

et al. 2014

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The existence of males and females, which are often strikingly different in morphology, reproductive strategies and behavior, is one of the most widespread phenomena in biology. However, the genetic mechanisms that generate this ubiquitous pattern are surprisingly diverse and do not follow a phylogenetic pattern. Sex-determination mechanisms can differ between even closely related species and arise frequently and independently. Fish provide a paradigmatic example, as their sex-determination mechanisms range from environmental to different modes of genetic determination. The evolutionary meaning of this remarkable plasticity is unknown. For genetic sex determination, where the trigger for female or male development comes from the genetic constitution of the individual, the evolution of sex-determination mechanisms is connected to a very peculiar genomic process, namely the formation of sex chromosomes [1][2][3][4] .To improve understanding of the function and evolution of sex chromosomes, their genetic organization must be deciphered.However, owing to their degenerate nature and high repetitive DNA content, sex chromosomes pose almost insurmountable problems in deciphering their gene content and organization. So far, only the human 5 , chimpanzee 6 and rhesus macaque Y chromosomes 7 and the male-specific region on the Y chromosome of one fish, the medaka 8 , have been sequenced. These analyses have nevertheless provided important insights into the evolution of Y chromosomes, their genomic organization and their degeneration processes, as well as predictions as to their likely evolutionary fate 9-12 .Much less genomic information exists on W chromosomes because, as with Y chromosomes, they are predominantly highly repetitive in nature. The prevailing theory of the evolution of sex chromosomes predicts that degeneration of the heterogametic sex chromosome is a stepwise process that occurs over an extended period of time. We therefore reasoned that an evolutionarily young W chromosome Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle Genetic sex determination by W and Z chromosomes has developed independently in different groups of organisms. To better understand the evolution of sex chromosomes and the plasticity of sex-determination mechanisms, we sequenced the whole genomes of a male (ZZ) and a female (ZW) half-smooth tongue sole (Cynoglossus semilaevis). In addition to insights into adaptation to a benthic lifestyle, we find that the sex chromosomes of these fish are derived from the same ancestral vertebrate protochromosome as the avian W and Z chromosomes. Notably, the same gene on the Z chromosome, dmrt1, which is the male-determining gene in birds, showed convergent evolution of features that are compatible with a similar function in tongue sole. Comparison of the relatively young tongue sole sex chromosomes with those of mammals and birds identified events that occurred during the early phase of sex-chromosome evolution. Pertinent to...

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“…First, information on the avian female-specific W chromosome, which is passed on from mothers to daughters, may influence yolk T transfer. Although the W chromosome contains only a few genes [34,35], it plays a key role in regulating female fertility and fecundity [11,12], probably through epistatic interactions between the W rspb.royalsocietypublishing.org Proc. R. Soc.…”

Section: Discussionmentioning

confidence: 99%

“…In line with these ideas, male-specific fitness traits, such as sperm motility [9] or spermatogenesis [10], are linked to the male-specific Y chromosome in species where the male is the heterogametic sex (XY). And similarly, in species where the female is the heterogametic sex (ZW), female fecundity and fertility traits are associated with the female-specific W chromosome [11,12].…”

Section: Introductionmentioning

confidence: 99%

Matrilineal inheritance of a key mediator of prenatal maternal effects

et al. 2016

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Sex-linkage is predicted to evolve in response to sex-specific or sexually antagonistic selection. In line with this prediction, most sex-linked genes are associated with reproduction in the respective sex. In addition to traits directly involved in fertility and fecundity, mediators of maternal effects may be predisposed to evolve sex-linkage, because they indirectly affect female fitness through their effect on offspring phenotype. Here, we test for sex-linked inheritance of a key mediator of prenatal maternal effects in oviparous species, the transfer of maternally derived testosterone to the eggs. Consistent with maternal inheritance, we found that in Japanese quail ( Coturnix japonica ) granddaughters resemble their maternal (but not their paternal) grandmother in yolk testosterone deposition. This pattern of resemblance was not due to non-genetic priming effects of testosterone exposure during prenatal development, as an experimental manipulation of yolk testosterone levels did not affect the females' testosterone transfer to their own eggs later in life. Instead, W chromosome and/or mitochondrial variation may underlie the observed matrilineal inheritance pattern. Ultimately, the inheritance of mediators of maternal effects along the maternal line will allow for a fast and direct response to female-specific selection, thereby affecting the dynamics of evolutionary processes mediated by maternal effects.

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W chromosome expression responds to female-specific selection

Cited by 98 publications

References 46 publications

Expansion of the Pseudo-autosomal Region and Ongoing Recombination Suppression in the Silene latifolia Sex Chromosomes

Expansion of the Pseudo-autosomal Region and Ongoing Recombination Suppression in the Silene latifolia Sex Chromosomes

Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle

Matrilineal inheritance of a key mediator of prenatal maternal effects

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