Spermatogenesis and the Evolution of Mammalian Sex Chromosomes

Larson, Erica L.; Kopania, Emily Emiko Konishi; Good, Jeffrey M.

doi:10.1016/j.tig.2018.06.003

Cited by 48 publications

(68 citation statements)

References 106 publications

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“…On the Drosophila Y chromosomes, all of the genes are specifically expressed in testes [ 15 , 16 , 17 ], and there is a dramatic increase of copy numbers of testis genes on the recently evolved Y chromosome of Drosophila as well [ 18 ]. In both mammals [ 19 ] and Drosophila [ 20 , 21 ], such ampliconic genes can vary across closely related species, likely due to the independent amplification on the Y chromosomes.…”

Section: Introductionmentioning

confidence: 99%

“…In addition, in organisms where the sex chromosomes are inactivated during meiosis, the demasculinization can be attributed to the evolutionary forces driving the testis-specific genes off the X chromosomes [ 27 ]. However, the genes expressed before the onset of meiotic sex chromosome inactivation can be overrepresented on the X chromosomes [ 19 , 28 ]. Moreover, recessive male-beneficial genes have a higher chance to accumulate on the X chromosomes that are favored by males [ 29 , 30 ].…”

Section: Introductionmentioning

confidence: 99%

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The Female-Specific W Chromosomes of Birds Have Conserved Gene Contents but Are Not Feminized

Zhou

2020

Genes

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Sex chromosomes are unique genomic regions with sex-specific or sex-biased inherent patterns and are expected to be more frequently subject to sex-specific selection. Substantial knowledge on the evolutionary patterns of sex-linked genes have been gained from the studies on the male heterogametic systems (XY male, XX female), but the understanding of the role of sex-specific selection in the evolution of female-heterogametic sex chromosomes (ZW female, ZZ male) is limited. Here we collect the W-linked genes of 27 birds, covering the three major avian clades: Neoaves (songbirds), Galloanserae (chicken), and Palaeognathae (ratites and tinamous). We find that the avian W chromosomes exhibit very conserved gene content despite their independent evolution of recombination suppression. The retained W-linked genes have higher dosage-sensitive and higher expression level than the lost genes, suggesting the role of purifying selection in their retention. Moreover, they are not enriched in ancestrally female-biased genes, and have not acquired new ovary-biased expression patterns after becoming W-linked. They are broadly expressed across female tissues, and the expression profile of the W-linked genes in females is not deviated from that of the homologous Z-linked genes. Together, our new analyses suggest that female-specific positive selection on the avian W chromosomes is limited, and the gene content of the W chromosomes is mainly shaped by purifying selection.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The Female-Specific W Chromosomes of Birds Have Conserved Gene Contents but Are Not Feminized

Zhou

2020

Genes

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“…In many species, compatibility is determined by one or more genetic loci that differ between compatible mating partners. The evolution of such genes has been studied in many systems including plants, animals, algae, and fungi [1,[4][5][6]. In animals and plants, genes that determine sexual compatibility are often found on sex chromosomes, which have distinct patterns of inheritance and diversification compared to autosomes [7].…”

Section: Introductionmentioning

confidence: 99%

Convergent evolution of linked mating-type loci in basidiomycete fungi

et al. 2019

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Sexual development is a key evolutionary innovation of eukaryotes. In many species, mating involves interaction between compatible mating partners that can undergo cell and nuclear fusion and subsequent steps of development including meiosis. Mating compatibility in fungi is governed by the mating type (MAT) loci. In basidiomycetes, the ancestral state is hypothesized to be tetrapolar, with two genetically unlinked MAT loci containing homeodomain transcription factor genes (HD locus) and pheromone and pheromone receptor genes (P/R locus), respectively. Alleles at both loci must differ between mating partners for completion of sexual development. However, there are also basidiomycetes with bipolar mating systems, which can arise through genomic linkage of the HD and P/R loci. In the order Tremellales, bipolarity is found only in the pathogenic Cryptococcus species. Here, we describe the analysis of MAT loci from 24 species of the Trichosporonales, a sister order to the Tremellales. In all of the species analyzed, the MAT loci are fused and a single HD gene is present in each mating type, similar to the organization in the pathogenic Cryptococci. However, the HD and P/R allele combinations in the Trichosporonales are different from those in the pathogenic Cryptococci. This and the existence of tetrapolar species in the Tremellales suggest that fusion of the HD and P/R loci occurred independently in the Trichosporonales and pathogenic Cryptococci, supporting the hypothesis of convergent evolution towards fused MAT regions, similar to previous findings in other fungal groups. Unlike the fused MAT loci in several other basidiomycete lineages though, the gene content and gene order within the fused MAT loci are highly conserved in the Trichosporonales, and there is no apparent suppression of recombination extending from the MAT loci to adjacent chromosomal regions, suggesting different mechanisms for the evolution of physically linked MAT loci in these groups.

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“…Similar to hybrid male sterility [109], the X chromosome also appears to play a central role in the genetic basis of mammalian hybrid inviability caused by placental dysplasia (Figure 1, [44,46,56]). Through these parallel systems of hybrid sterility and inviability, a trend is emerging where sex chromosome evolution and genetic conflict within regulatory systems appears to fuel divergence within these key developmental processes [110,111], ultimately leading to the formation of reproductive barriers between species.…”

Section: Normal F1mentioning

confidence: 99%

X chromosome-dependent disruption of placental regulatory networks in hybrid dwarf hamsters

Brekke

Moore

Campbell‐Staton

et al. 2020

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Disruption of placental gene expression contributes to several congenital developmental disorders in humans, and may play an important role in the evolution of reproductive barriers between species. The placenta is also highly enriched for interacting genes showing parent-of-origin or imprinted expression, which is thought to have evolved to mitigate parental conflict within this extra-embryonic tissue. However, relatively little is known about the broader organization, functional integration, and evolution of placental gene expression networks across species. Here we used a systems genetics approach to examine the genetic and regulatory underpinnings of placental overgrowth in hybrids between two species of dwarf hamsters (Phodopus sungorus and P. campbelli). Using quantitative genetic mapping and mitochondrial substitution lines, we show that the X chromosome is the major maternal factor explaining massive parent-of-origin dependent placental overgrowth in hybrids. Mitochondrial interactions did not contribute to abnormal hybrid placental development, and there was only weak correspondence between placental disruption and early embryonic growth phenotypes. In parallel, genome-wide analyses of placental transcriptomes from the parental species and first and second-generation hybrids revealed a central group of co-expressed X-linked and autosomal genes that were highly enriched for maternally-biased expression. Expression of this core placental regulatory network was strongly correlated with placental growth and showed widespread misexpression dependent on epistatic interactions with X-linked hybrid incompatibilities. Silencing of the paternal X chromosome and most candidate paternally imprinted autosomal genes appeared unperturbed in the same genetic crosses. Collectively, our results indicate that the X chromosome plays a prominent role in the evolution of placental gene expression and the rapid accumulation of hybrid developmental barriers between mammalian species.

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Spermatogenesis and the Evolution of Mammalian Sex Chromosomes

Cited by 48 publications

References 106 publications

The Female-Specific W Chromosomes of Birds Have Conserved Gene Contents but Are Not Feminized

The Female-Specific W Chromosomes of Birds Have Conserved Gene Contents but Are Not Feminized

Convergent evolution of linked mating-type loci in basidiomycete fungi

X chromosome-dependent disruption of placental regulatory networks in hybrid dwarf hamsters

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