Multiple and Independent Cessation of Recombination Between Avian Sex Chromosomes

Abstract Birds are characterized by female heterogamety; females carry the Z and W sex chromosomes, while males have two copies of the Z chromosome. We suggest here that full differentiation of the Z and W sex chromosomes of birds did not take place until after the split of major contemporary lineages, in the late Cretaceous. The ATP synthase α-subunit gene is now present in one copy each on the nonrecombining part of the W chromosome (ATP5A1W) and on the Z chromosome (ATP5A1Z). This gene seems to have evolved on several independent occasions, in different lineages, from a state of free recombination into two sex-specific and nonrecombining variants. ATP5A1W and ATP5A1Z are thus more similar within orders, relative to what W (or Z) are between orders. Moreover, this cessation of recombination apparently took place at different times in different lineages (estimated at 13, 40, and 65 million years ago in Ciconiiformes, Galliformes, and Anseriformes, respectively). We argue that these observations are the result of recent and traceable steps in the process where sex chromosomes gradually cease to recombine and become differentiated. Our data demonstrate that this process, once initiated, may occur independently in parallel in sister lineages.

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Genetic sex determination and sex-specific lifespan in tetrapods – evidence of a toxic Y effect

10.1101/2020.03.09.983700 ◽

2020 ◽

Author(s):

Zahida Sultanova ◽

Philip A. Downing ◽

Pau Carazo

Keyword(s):

Sex Chromosomes ◽

Alternative Hypothesis ◽

Z Chromosome ◽

W Chromosome ◽

Deleterious Mutations ◽

Recessive Mutations ◽

Y Chromosomes ◽

Heterogametic Sex ◽

Taxonomic Patterns

ABSTRACTSex-specific lifespans are ubiquitous across the tree of life and exhibit broad taxonomic patterns that remain a puzzle, such as males living longer than females in birds and vice versa in mammals. The prevailing “unguarded-X” hypothesis (UXh) explains this by differential expression of recessive mutations in the X/Z chromosome of the heterogametic sex (e.g., females in birds and males in mammals), but has only received indirect support to date. An alternative hypothesis is that the accumulation of deleterious mutations and repetitive elements on the Y/W chromosome might lower the survival of the heterogametic sex (“toxic Y” hypothesis). Here, we report lower survival of the heterogametic relative to the homogametic sex across 138 species of birds, mammals, reptiles and amphibians, as expected if sex chromosomes shape sex-specific lifespans. We then analysed bird and mammal karyotypes and found that the relative sizes of the X and Z chromosomes are not associated with sex-specific lifespans, contrary to UXh predictions. In contrast, we found that Y size correlates negatively with male survival in mammals, where toxic Y effects are expected to be particularly strong. This suggests that small Y chromosomes benefit male lifespans. Our results confirm the role of sex chromosomes in explaining sex differences in lifespan, but indicate that, at least in mammals, this is better explained by “toxic Y” rather than UXh effects.

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Male-Biased Mutation Rates Revealed from Z and W Chromosome-Linked ATP Synthase α-Subunit (ATP5A1) Sequences in Birds

Journal of Molecular Evolution ◽

10.1007/s002390010046 ◽

2000 ◽

Vol 50 (5) ◽

pp. 443-447 ◽

Cited By ~ 30

Author(s):

Ariane N. Carmichael ◽

Anna-Karin Fridolfsson ◽

Joy Halverson ◽

Hans Ellegren

Keyword(s):

Atp Synthase ◽

Mutation Rates ◽

W Chromosome ◽

Α Subunit

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A frog with three sex chromosomes that co-mingle together in nature: Xenopus tropicalis has a degenerate W and a Y that evolved from a Z chromosome

PLoS Genetics ◽

10.1371/journal.pgen.1009121 ◽

2020 ◽

Vol 16 (11) ◽

pp. e1009121

Author(s):

Benjamin L. S. Furman ◽

Caroline M. S. Cauret ◽

Martin Knytl ◽

Xue-Ying Song ◽

Tharindu Premachandra ◽

...

Keyword(s):

Sex Differences ◽

Y Chromosome ◽

Sex Chromosomes ◽

Sexual Differentiation ◽

Sex Chromosome ◽

Xenopus Tropicalis ◽

Z Chromosome ◽

W Chromosome ◽

Recombination Suppression ◽

Determining Factor

In many species, sexual differentiation is a vital prelude to reproduction, and disruption of this process can have severe fitness effects, including sterility. It is thus interesting that genetic systems governing sexual differentiation vary among—and even within—species. To understand these systems more, we investigated a rare example of a frog with three sex chromosomes: the Western clawed frog, Xenopus tropicalis. We demonstrate that natural populations from the western and eastern edges of Ghana have a young Y chromosome, and that a male-determining factor on this Y chromosome is in a very similar genomic location as a previously known female-determining factor on the W chromosome. Nucleotide polymorphism of expressed transcripts suggests genetic degeneration on the W chromosome, emergence of a new Y chromosome from an ancestral Z chromosome, and natural co-mingling of the W, Z, and Y chromosomes in the same population. Compared to the rest of the genome, a small sex-associated portion of the sex chromosomes has a 50-fold enrichment of transcripts with male-biased expression during early gonadal differentiation. Additionally, X. tropicalis has sex-differences in the rates and genomic locations of recombination events during gametogenesis that are similar to at least two other Xenopus species, which suggests that sex differences in recombination are genus-wide. These findings are consistent with theoretical expectations associated with recombination suppression on sex chromosomes, demonstrate that several characteristics of old and established sex chromosomes (e.g., nucleotide divergence, sex biased expression) can arise well before sex chromosomes become cytogenetically distinguished, and show how these characteristics can have lingering consequences that are carried forward through sex chromosome turnovers.

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Evolutionary Variability of W-Linked Repetitive Content in Lacertid Lizards

Genes ◽

10.3390/genes11050531 ◽

2020 ◽

Vol 11 (5) ◽

pp. 531

Author(s):

Grzegorz Suwala ◽

Marie Altmanová ◽

Sofia Mazzoleni ◽

Emmanouela Karameta ◽

Panayiotis Pafilis ◽

...

Keyword(s):

Sex Chromosomes ◽

Sex Chromosome ◽

Phylogenetic Signal ◽

Z Chromosome ◽

Specific Gene ◽

W Chromosome ◽

Squamate Reptiles ◽

Lacertid Lizards ◽

Species Specific

Lacertid lizards are a widely radiated group of squamate reptiles with long-term stable ZZ/ZW sex chromosomes. Despite their family-wide homology of Z-specific gene content, previous cytogenetic studies revealed significant variability in the size, morphology, and heterochromatin distribution of their W chromosome. However, there is little evidence about the accumulation and distribution of repetitive content on lacertid chromosomes, especially on their W chromosome. In order to expand our knowledge of the evolution of sex chromosome repetitive content, we examined the topology of telomeric and microsatellite motifs that tend to often accumulate on the sex chromosomes of reptiles in the karyotypes of 15 species of lacertids by fluorescence in situ hybridization (FISH). The topology of the above-mentioned motifs was compared to the pattern of heterochromatin distribution, as revealed by C-banding. Our results show that the topologies of the examined motifs on the W chromosome do not seem to follow a strong phylogenetic signal, indicating independent and species-specific accumulations. In addition, the degeneration of the W chromosome can also affect the Z chromosome and potentially also other parts of the genome. Our study provides solid evidence that the repetitive content of the degenerated sex chromosomes is one of the most evolutionary dynamic parts of the genome.

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Expression of the Drosophila melanogaster ATP synthase α subunit gene is regulated by a transcriptional element containing GAF and Adf-1 binding sites

European Journal of Biochemistry ◽

10.1111/j.1432-1033.2004.04336.x ◽

2004 ◽

Vol 271 (20) ◽

pp. 4003-4013 ◽

Cited By ~ 7

Author(s):

Ana Talamillo ◽

Miguel Angel Fernández-Moreno ◽

Francisco Martínez-Azorín ◽

Belén Bornstein ◽

Pilar Ochoa ◽

...

Keyword(s):

Drosophila Melanogaster ◽

Atp Synthase ◽

Binding Sites ◽

Subunit Gene ◽

Α Subunit

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Molecular Evolution of the Avian CHD1 Genes on the Z and W Sex Chromosomes

Genetics ◽

10.1093/genetics/155.4.1903 ◽

2000 ◽

Vol 155 (4) ◽

pp. 1903-1912 ◽

Cited By ~ 2

Author(s):

Anna-Karin Fridolfsson ◽

Hans Ellegren

Keyword(s):

Molecular Evolution ◽

Sex Chromosomes ◽

Sequence Data ◽

Neutral Evolution ◽

Z Chromosome ◽

W Chromosome ◽

Effective Population ◽

Synonymous Substitutions ◽

Nonsynonymous Substitutions ◽

Female Specific

Abstract Genes shared between the nonrecombining parts of the two types of sex chromosomes offer a potential means to study the molecular evolution of the same gene exposed to different genomic environments. We have analyzed the molecular evolution of the coding sequence of the first pair of genes found to be shared by the avian Z (present in both sexes) and W (female-specific) sex chromosomes, CHD1Z and CHD1W. We show here that these two genes evolve independently but are highly conserved at nucleotide as well as amino acid levels, thus not indicating a female-specific role of the CHD1W gene. From comparisons of sequence data from three avian lineages, the frequency of nonsynonymous substitutions (Ka) was found to be higher for CHD1W (1.55 per 100 sites) than for CHD1Z (0.81), while the opposite was found for synonymous substitutions (Ks, 13.5 vs. 22.7). We argue that the lower effective population size and the absence of recombination on the W chromosome will generally imply that nonsynonymous substitutions accumulate faster on this chromosome than on the Z chromosome. The same should be true for the Y chromosome relative to the X chromosome in XY systems. Our data are compatible with a male-biased mutation rate, manifested by the faster rate of neutral evolution (synonymous substitutions) on the Z chromosome than on the female-specific W chromosome.

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Loss of the Gene for the α Subunit of ATP Synthase (ATP5A1) from the W Chromosome in the African Grey Parrot (Psittacus erithacus)

Journal of Molecular Evolution ◽

10.1007/s002390010201 ◽

2001 ◽

Vol 53 (2) ◽

pp. 135-143 ◽

Cited By ~ 7

Author(s):

Siwo R. de Kloet

Keyword(s):

Atp Synthase ◽

W Chromosome ◽

Α Subunit ◽

African Grey Parrot ◽

Psittacus Erithacus ◽

Grey Parrot

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Sex chromosome pairing and sex chromatin bodies in W–Z translocation strains of Ephestia kuehniella (Lepidoptera)

Genome ◽

10.1139/g94-060 ◽

1994 ◽

Vol 37 (3) ◽

pp. 426-435 ◽

Cited By ~ 27

Author(s):

František Marec ◽

Walther Traut

Keyword(s):

Chromosome Pairing ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Ephestia Kuehniella ◽

Z Chromosome ◽

W Chromosome ◽

Wild Type ◽

Electron Microscopic ◽

Sex Chromatin ◽

Mediterranean Flour Moth

Structure and pairing behavior of sex chromosomes in females of four T(W;Z) lines of the Mediterranean flour moth, Ephestia kuehniella, were investigated using light and electron microscopic techniques and compared with the wild type. In light microscopic preparations of pachytene oocytes of wild-type females, the WZ bivalent stands out by its heterochromatic W chromosome strand. In T(W;Z) females, the part of the Z chromosome that was translated onto the W chromosome was demonstrated as a distal segment of the neo-W chromosome, displaying a characteristic non-W chromosomal chromomere–interchromomere pattern. This segment is homologously paired with the corresponding part of a complete Z chromosome. In contrast with the single ball of heterochromatic W chromatin in highly polyploid somatic nuclei of wild-type females, the translocation causes the formation of deformed or fragmented W chromatin bodies, probably owing to opposing tendencies of the Z and W chromosomal parts of the neo-W. In electron microscopic preparations of microspread nuclei, sex chromosome bivalents were identified by the remnants of electron-dense heterochromatin tangles decorating the W chromosome axis, by the different lengths of the Z and W chromosome axes, and by incomplete pairing. No heterochromatin tangles were attached to the translocated segment of the Z chromosome at one end of the neo-W chromosome. Because of the homologous pairing between the translocation and the structurally normal Z chromosome, pairing affinity of sex chromosomes in T(W;Z) females is significantly improved. Specific differences observed among T(W;Z)1–4 translocations are probably due to the different lengths of the translocated segments.Key words: Mediterranean flour moth, sex chromosomes, sex chromatin, translocations, synaptonemal complexes, microspreading.

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Identification of sex chromosomes in Eremias velox (Lacertidae, Reptilia) using lampbrush chromosome analysis

Comparative Cytogenetics ◽

10.3897/compcytogen.v13i2.34116 ◽

2019 ◽

Vol 13 (2) ◽

pp. 17-28

Author(s):

Artem P. Lisachov ◽

Svetlana A. Galkina ◽

Alsu F. Saifitdinova ◽

Svetlana A. Romanenko ◽

Daria A. Andreyushkova ◽

...

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Chromosome Analysis ◽

Lampbrush Chromosome ◽

Z Chromosome ◽

Specific Probe ◽

W Chromosome ◽

Lacertid Lizards ◽

Genomic Studies ◽

Active Transcription

Reptiles are good objects for studying the evolution of sex determination, since they have different sex determination systems in different lineages. Lacertid lizards have been long-known for possessing ZZ/ZW type sex chromosomes. However, due to morphological uniformity of lacertid chromosomes, the Z chromosome has been only putatively cytologically identified. We used lampbrush chromosome (LBC) analysis and FISH with a W-specific probe in Eremiasvelox (Pallas, 1771) to unequivocally identify the ZW bivalent and investigate its meiotic behavior. The heterochromatic W chromosome is decondensed at the lampbrush stage, indicating active transcription, contrast with the highly condensed condition of the lampbrush W chromosomes in birds. We identified the Z chromosome by its chiasmatic association with the W chromosome as chromosome XIII of the 19 chromosomes in the LBC karyotype. Our findings agree with previous genetic and genomic studies, which suggested that the lacertid Z chromosome should be one of the smaller macrochromosomes.

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