Evolutionary Diversity and Turn-Over of Sex Determination in Teleost Fishes

Mank, Judith E.; Avise, John C.

doi:10.1159/000223071

Cited by 169 publications

(145 citation statements)

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“…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. We determined the age of the tongue sole sex chromosomes to be about 30 million years (Supplementary Table 31), which is consistent with the general view that fish have young sex chromosomes [13][14][15] . This age contrasts with the hundreds of millions of years for the ancestry of the mammalian Y and avian W chromosomes 1,41 and could serve to explain why there are still many intact genes in the non-recombining region of the tongue sole W chromosome.…”

Section: Genomic Organization and Evolution Of Z And Wsupporting

confidence: 76%

“…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 A r t i c l e s should be more amenable for sequencing than the highly degenerated, up to 200-million-year-old W chromosome of birds and would also provide insights into the early steps of W-chromosome evolution. Fish have long been known to have relatively young sex chromosomes [13][14][15] . We selected a flatfish for our study on the basis that these fish would have young sex chromosomes and offer the advantage of a relatively small genome, one that is not much larger than that of pufferfishes.…”

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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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Section: Genomic Organization and Evolution Of Z And Wsupporting

confidence: 76%

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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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“…However, the mechanism by which the sex differentiation pathway is triggered varies widely (Marin and Baker, 1998;Herpin and Schartl, 2011). The fact that two different regions determine sex in closely related species of Cottus indicates that factors controlling a conserved sex determination pathway evolve rapidly and have a fast turnover, which is not astonishing given the results from other fish species (Mank and Avise, 2009). Detailed genetic studies will have to reveal whether the same genes are repeatedly recruited in different lineages.…”

Section: Discussionmentioning

confidence: 99%

The genomics of incompatibility factors and sex determination in hybridizing species of Cottus (Pisces)

2013

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Cottus rhenanus and Cottus perifretum have formed hybrid lineages and narrow hybrid zones that can be best explained through the action of natural selection. However, the underlying selective forces as well as their genomic targets are not well understood. This study identifies genomic regions in the parental species that cause hybrid incompatibilities and tests whether these manifest in a sex-specific manner to learn about processes that affect natural hybridization in Cottus. Interspecific F 2 crosses were analyzed for 255 markers for genetic mapping and to detect transmission distortion as a sign for genetic incompatibilities. The Cottus map consists of 24 linkage groups with a total length of 1575.4 cM. A male heterogametic (XY) sex determination region was found on different linkage groups in the two parental species. Genetic incompatibilities were incomplete, varied among individuals and populations and were not associated with the heterogametic sex. The variance between populations and individuals makes it unlikely that there are species-specific incompatibility loci that could affect the gene pool of natural hybrids in a simple and predictable way. Conserved synteny with sequenced fish genomes permits to genetically study the Cottus genome through the transfer of genomic information from the model fish species. Homology relationships of candidate genomic regions in Cottus indicate that sex determination is not based on the same genomic regions found in other fish species. This suggests a fast evolutionary turnover of the genetic basis of sex determination that, together with the small size of the heterogametic regions, may contribute to the absence of fitness effects related to the Haldane's rule.

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“…Note that sex chromosomes in fish are mostly homomorphic and not differentiated (Ohno 1974), which is in contrast to the degenerated Y and W chromosomes in mammals (Graves 2006) and birds (Takagi and Sasaki 1974), respectively. This is one possible explanation for the viable combination of different sex chromosomal systems within a single species or population of fish (Parnell and Streelman 2013) and could be a mechanistic reason why sex chromosome turnovers occur easily and frequently in this group (Mank and Avise 2009). Additionally, fish can have more complex sex chromosomal systems involving more than one chromosome pair (see Figure 2).…”

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Genetics of Sexual Development: An Evolutionary Playground for Fish

2014

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Teleost fishes are the most species-rich clade of vertebrates and feature an overwhelming diversity of sex-determining mechanisms, classically grouped into environmental and genetic systems. Here, we review the recent findings in the field of sex determination in fish. In the past few years, several new master regulators of sex determination and other factors involved in sexual development have been discovered in teleosts. These data point toward a greater genetic plasticity in generating the male and female sex than previously appreciated and implicate novel gene pathways in the initial regulation of the sexual fate. Overall, it seems that sex determination in fish does not resort to a single genetic cascade but is rather regulated along a continuum of environmental and heritable factors.

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Evolutionary Diversity and Turn-Over of Sex Determination in Teleost Fishes

Cited by 169 publications

References 163 publications

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

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

The genomics of incompatibility factors and sex determination in hybridizing species of Cottus (Pisces)

Genetics of Sexual Development: An Evolutionary Playground for Fish

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