Evolutionary Variability of W-Linked Repetitive Content in Lacertid Lizards

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.

Download Full-text

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.

Download Full-text

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.

Download Full-text

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.

Download Full-text

Evaluation of Four Methods to Identify the Homozygotic Sex Chromosome in Small Populations

10.21203/rs.3.rs-892602/v1 ◽

2021 ◽

Author(s):

Charles Christian Riis Hansen ◽

Kristen M. Westfall ◽

Snaebjörn Pálsson

Keyword(s):

Sex Chromosomes ◽

Sex Chromosome ◽

Read Depth ◽

Mapping Method ◽

Small Population ◽

Genomic Variation ◽

Z Chromosome ◽

Effective Population ◽

Organelle Genomes ◽

Heterogametic Sex

Abstract BackgroundWhole genomes are commonly assembled into a collection of scaffolds and often lack annotations of autosomes, sex chromosomes, and organelle genomes (i.e., mitochondrial and chloroplast). As these chromosome types differ in effective population size and can have highly disparate evolutionary histories, it is imperative to take this information into account when analysing genomic variation. Here we assessed the accuracy of four methods for identifying the homogametic sex chromosome in a small population using two whole genome sequences (WGS) and 133 RAD sequences of white-tailed eagles (Haliaeetus albicilla): i) difference in read depth per scaffold in a male and a female, ii) heterozygosity per scaffold in a male and a female, iii) mapping to a reference genome of a related species (chicken) with identified sex chromosomes, and iv) analysis of SNP-loadings from a principal components analysis (PCA), based on the low-depth RADseq data. ResultsThe best performing approach was the reference mapping (method iii), which identified 98.12% of the expected homogametic sex chromosome (Z). The read depth per scaffold (method i) identified 86.41% of the homogametic sex chromosome with few false positives. The SNP-loading scores (method iv) found 78.6% of the Z-chromosome and had a false positive discovery rate of more than 10%. The heterozygosity per scaffold (method ii) did not provide clear results due to a lack of diversity in both the Z and autosomal chromosomes, and potential interference from the heterogametic sex chromosome (W). The evaluation of these methods also revealed 10 Mb of likely PAR and gametologous regions.ConclusionIdentification of the homogametic sex chromosome in a small population is best accomplished by reference mapping or examining read depth differences between sexes.

Download Full-text

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.

Download Full-text

Evolutionary Dynamics of Sex Chromosomes of Paleognathous Birds

Genome Biology and Evolution ◽

10.1093/gbe/evz154 ◽

2019 ◽

Vol 11 (8) ◽

pp. 2376-2390 ◽

Cited By ~ 13

Author(s):

Luohao Xu ◽

Simon Yung Wa Sin ◽

Phil Grayson ◽

Scott V Edwards ◽

Timothy B Sackton

Keyword(s):

Sex Chromosomes ◽

Evolutionary Dynamics ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Z Chromosome ◽

Recombination Suppression ◽

Evolutionary Forces ◽

Genomic Level ◽

Standard Models ◽

Pseudoautosomal Regions

Abstract Standard models of sex chromosome evolution propose that recombination suppression leads to the degeneration of the heterogametic chromosome, as is seen for the Y chromosome in mammals and the W chromosome in most birds. Unlike other birds, paleognaths (ratites and tinamous) possess large nondegenerate regions on their sex chromosomes (PARs or pseudoautosomal regions). It remains unclear why these large PARs are retained over >100 Myr, and how this retention impacts the evolution of sex chromosomes within this system. To address this puzzle, we analyzed Z chromosome evolution and gene expression across 12 paleognaths, several of whose genomes have recently been sequenced. We confirm at the genomic level that most paleognaths retain large PARs. As in other birds, we find that all paleognaths have incomplete dosage compensation on the regions of the Z chromosome homologous to degenerated portions of the W (differentiated regions), but we find no evidence for enrichments of male-biased genes in PARs. We find limited evidence for increased evolutionary rates (faster-Z) either across the chromosome or in differentiated regions for most paleognaths with large PARs, but do recover signals of faster-Z evolution in tinamou species with mostly degenerated W chromosomes, similar to the pattern seen in neognaths. Unexpectedly, in some species, PAR-linked genes evolve faster on average than genes on autosomes, suggested by diverse genomic features to be due to reduced efficacy of selection in paleognath PARs. Our analysis shows that paleognath Z chromosomes are atypical at the genomic level, but the evolutionary forces maintaining largely homomorphic sex chromosomes in these species remain elusive.

Download Full-text

Codling moth cytogenetics: karyotype, chromosomal location of rDNA, and molecular differentiation of sex chromosomes

Genome ◽

10.1139/g05-063 ◽

2005 ◽

Vol 48 (6) ◽

pp. 1083-1092 ◽

Cited By ~ 71

Author(s):

Iva Fuková ◽

Petr Nguyen ◽

František Marec

Keyword(s):

Sex Chromosomes ◽

Sex Chromosome ◽

Codling Moth ◽

Dna Probe ◽

Rrna Genes ◽

Comparative Genomic ◽

W Chromosome ◽

Genomic Hybridization ◽

Molecular Differentiation ◽

Sex Chromatin

We performed a detailed karyotype analysis in the codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae), the key pest of pome fruit in the temperate regions of the world. The codling moth karyotype consisted of 2n = 56 chromosomes of a holokinetic type. The chromosomes were classified into 5 groups according to their sizes: extra large (3 pairs), large (3 pairs), medium (15 pairs), small (5 pairs), and dot-like (2 pairs). In pachytene nuclei of both sexes, a curious NOR (nucleolar organizer region) bivalent was observed. It carried 2 nucleoli, each associated with one end of the bivalent. FISH with an 18S ribosomal DNA probe confirmed the presence of 2 clusters of rRNA genes at the opposite ends of the bivalent. In accordance with this finding, 2 homologous NOR chromosomes were identified in mitotic metaphase, each showing hybridization signals at both ends. In highly polyploid somatic nuclei, females showed a large heterochromatin body, the so-called sex chromatin or W chromatin. The heterochromatin body was absent in male nuclei, indicating a WZ/ZZ (female/male) sex chromosome system. In keeping with the sex chromatin status, pachytene oocytes showed a sex chromosome bivalent (WZ) that was easily discernible by its heterochromatic W thread. To study molecular differentiation of the sex chromosomes, we employed genomic in situ hybridization (GISH) and comparative genomic hybridization (CGH). GISH detected the W chromosome by strong binding of the Cy3-labelled, female-derived DNA probe. With CGH, both the Cy3-labelled female-derived probe and Fluor-X labelled male-derived probe evenly bound to the W chromosome. This suggested that the W chromosome is predominantly composed of repetitive DNA sequences occurring scattered in other chromosomes but accumulated in the W chromosome. The demonstrated ways of W chromosome identification will facilitate the development of genetic sexing strains desirable for pest control using the sterile insect technique.Key words: CGH, codling moth, FISH, GISH, genomic hybridization, heterochromatin, holokinetic chromosomes, karyotype, NOR, rDNA, SIT, sex chromosomes.

Download Full-text

Snake W Sex Chromosome: The Shadow of Ancestral Amniote Super-Sex Chromosome

Cells ◽

10.3390/cells9112386 ◽

2020 ◽

Vol 9 (11) ◽

pp. 2386

Author(s):

Worapong Singchat ◽

Syed Farhan Ahmad ◽

Nararat Laopichienpong ◽

Aorarat Suntronpong ◽

Thitipong Panthum ◽

...

Keyword(s):

Sex Chromosomes ◽

Evolutionary Dynamics ◽

Sex Chromosome ◽

Chromosomal Rearrangements ◽

Chromosome Analysis ◽

Chromosome Conformation ◽

Principal Mechanism ◽

Squamate Reptiles ◽

Genomic Landscape ◽

Heteromorphic Sex Chromosomes

Heteromorphic sex chromosomes, particularly the ZZ/ZW sex chromosome system of birds and some reptiles, undergo evolutionary dynamics distinct from those of autosomes. The W sex chromosome is a unique karyological member of this heteromorphic pair, which has been extensively studied in snakes to explore the origin, evolution, and genetic diversity of amniote sex chromosomes. The snake W sex chromosome offers a fascinating model system to elucidate ancestral trajectories that have resulted in genetic divergence of amniote sex chromosomes. Although the principal mechanism driving evolution of the amniote sex chromosome remains obscure, an emerging hypothesis, supported by studies of W sex chromosomes of squamate reptiles and snakes, suggests that sex chromosomes share varied genomic blocks across several amniote lineages. This implies the possible split of an ancestral super-sex chromosome via chromosomal rearrangements. We review the major findings pertaining to sex chromosomal profiles in amniotes and discuss the evolution of an ancestral super-sex chromosome by collating recent evidence sourced mainly from the snake W sex chromosome analysis. We highlight the role of repeat-mediated sex chromosome conformation and present a genomic landscape of snake Z and W chromosomes, which reveals the relative abundance of major repeats, and identifies the expansion of certain transposable elements. The latest revolution in chromosomics, i.e., complete telomere-to-telomere assembly, offers mechanistic insights into the evolutionary origin of sex chromosomes.

Download Full-text

Karyotype Evolution and Distinct Evolutionary History of the W Chromosomes in Swallows (Aves, Passeriformes)

Cytogenetic and Genome Research ◽

10.1159/000500621 ◽

2019 ◽

Vol 158 (2) ◽

pp. 98-105 ◽

Cited By ~ 3

Author(s):

Suziane A. Barcellos ◽

Rafael Kretschmer ◽

Marcelo S. de Souza ◽

Alice L. Costa ◽

Tiago M. Degrandi ◽

...

Keyword(s):

Dna Sequences ◽

Evolutionary History ◽

Karyotype Evolution ◽

Sex Chromosome ◽

Repetitive Sequences ◽

Z Chromosome ◽

W Chromosome ◽

The Family ◽

Agnor Staining ◽

History Of

As in many other bird groups, data on karyotype organization and distribution of repetitive sequences are also lacking in species belonging to the family Hirundinidae. Thus, in the present study, we analyzed the karyotypes of 3 swallow species (Progne tapera, Progne chalybea, and Pygochelidon cyanoleuca) by Giemsa and AgNOR staining, C-banding, and FISH with 11 microsatellite sequences. The diploid chromosome number was 2n = 76 in all 3 species, and NORs were observed in 2 chromosome pairs each. The microsatellite distribution pattern was similar in both Progne species, whereas P. cyanoleuca presented a distinct organization. These repetitive DNA sequences were found in the centromeric, pericentromeric, and telomeric regions of the macrochromosomes, as well as in 2 interstitial blocks in the W chromosome. Most microchromosomes had mainly telomeric signals. The Z chromosome displayed 1 hybridization signal in P. tapera but none in the other species. In contrast, the W chromosome showed an accumulation of different microsatellite sequences. The swallow W chromosome is larger than that of most Passeriformes. The observed enlargement in chromosome size might be explained by these high amounts of repetitive sequences. In sum, our data highlight the significant role that microsatellite sequences may play in sex chromosome differentiation.

Download Full-text

Chromosomal Spreading of Microsatellites and (TTAGGG)n Sequences in the Characidium zebra and C. gomesi Genomes (Characiformes: Crenuchidae)

Cytogenetic and Genome Research ◽

10.1159/000447959 ◽

2016 ◽

Vol 149 (3) ◽

pp. 182-190 ◽

Cited By ~ 12

Author(s):

Marcela B. Pucci ◽

Patricia Barbosa ◽

Viviane Nogaroto ◽

Mara C. Almeida ◽

Roberto F. Artoni ◽

...

Keyword(s):

Repetitive Dna ◽

Sex Chromosomes ◽

Dna Sequences ◽

Tandem Repeats ◽

Additional Data ◽

Sex Chromosome ◽

Binding Motif ◽

W Chromosome ◽

Repeat Sequences ◽

Heteromorphic Sex Chromosomes

Sex chromosome evolution involves the accumulation of repeat sequences such as multigenic families, noncoding repetitive DNA (satellite, minisatellite, and microsatellite), and mobile elements such as transposons and retrotransposons. Most species of Characidium exhibit heteromorphic ZZ/ZW sex chromosomes; the W is characterized by an intense accumulation of repetitive DNA including dispersed satellite DNA sequences and transposable elements. The aim of this study was to analyze the distribution pattern of 18 different tandem repeats, including (GATA)n and (TTAGGG)n, in the genomes of C. zebra and C. gomesi, especially in the C. gomesi W chromosome. In the C. gomesi W chromosome, weak signals were seen for (CAA)10, (CAC)10, (CAT)10, (CGG)10, (GAC)10, and (CA)15 probes. (GA)15 and (TA)15 hybridized to the autosomes but not to the W chromosome. The (GATA)n probe hybridized to the short arms of the W chromosome as well as the (CG)15 probe. The (GATA)n repeat is known to be a protein-binding motif. GATA-binding proteins are necessary for the decondensation of heterochromatic regions that hold coding genes, especially in some heteromorphic sex chromosomes that may keep genes related to oocyte development. The (TAA)10 repeat is accumulated in the entire W chromosome, and this microsatellite accumulation is probably involved in the sex chromosome differentiation process and crossover suppression in C. gomesi. These additional data on the W chromosome DNA composition help to explain the evolution of sex chromosomes in Characidium.

Download Full-text