The Staurotypus Turtles and Aves Share the Same Origin of Sex Chromosomes but Evolved Different Types of Heterogametic Sex Determination

Frogs are ideal organisms for studying sex chromosome evolution because of their diversity in sex chromosome differentiation and sex-determination systems. We review 222 anuran frogs, spanning ~220 Myr of divergence, with characterized sex chromosomes, and discuss their evolution, phylogenetic distribution and transitions between homomorphic and heteromorphic states, as well as between sex-determination systems. Most (~75%) anurans have homomorphic sex chromosomes, with XY systems being three times more common than ZW systems. Most remaining anurans (~25%) have heteromorphic sex chromosomes, with XY and ZW systems almost equally represented. There are Y-autosome fusions in 11 species, and no W-/Z-/X-autosome fusions are known. The phylogeny represents at least 19 transitions between sex-determination systems and at least 16 cases of independent evolution of heteromorphic sex chromosomes from homomorphy, the likely ancestral state. Five lineages mostly have heteromorphic sex chromosomes, which might have evolved due to demographic and sexual selection attributes of those lineages. Males do not recombine over most of their genome, regardless of which is the heterogametic sex. Nevertheless, telomere-restricted recombination between ZW chromosomes has evolved at least once. More comparative genomic studies are needed to understand the evolutionary trajectories of sex chromosomes among frog lineages, especially in the ZW systems.

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Change of the Heterogametic Sex From Male to Female in the Frog

Genetics ◽

10.1093/genetics/164.2.613 ◽

2003 ◽

Vol 164 (2) ◽

pp. 613-620 ◽

Cited By ~ 1

Author(s):

M Ogata ◽

H Ohtani ◽

T Igarashi ◽

Y Hasegawa ◽

Y Ichikawa ◽

...

Keyword(s):

Sex Chromosomes ◽

Sex Chromosome ◽

Hybrid Population ◽

12S Rrna ◽

Rrna Gene ◽

The West ◽

Male Bias ◽

Different Types ◽

Heterogametic Sex ◽

Male To Female

Abstract Two different types of sex chromosomes, XX/XY and ZZ/ZW, exist in the Japanese frog Rana rugosa. They are separated in two local forms that share a common origin in hybridization between the other two forms (West Japan and Kanto) with male heterogametic sex determination and homomorphic sex chromosomes. In this study, to find out how the different types of sex chromosomes differentiated, particularly the evolutionary reason for the heterogametic sex change from male to female, we performed artificial crossings between the West Japan and Kanto forms and mitochondrial 12S rRNA gene sequence analysis. The crossing results showed male bias using mother frogs with West Japan cytoplasm and female bias using those with Kanto cytoplasm. The mitochondrial genes of ZZ/ZW and XX/XY forms, respectively, were similar in sequence to those of the West Japan and Kanto forms. These results suggest that in the primary ZZ/ZW form, the West Japan strain was maternal and thus male bias was caused by the introgression of the Kanto strain while in the primary XX/XY form and vice versa. We therefore hypothesize that sex ratio bias according to the maternal origin of the hybrid population was a trigger for the sex chromosome differentiation and the change of heterogametic sex.

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Unusual sex chromosome inheritance in mammals

Philosophical Transactions of the Royal Society of London Series B Biological Sciences ◽

10.1098/rstb.1970.0042 ◽

1970 ◽

Vol 259 (828) ◽

pp. 15-36 ◽

Cited By ~ 66

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Sex Chromosome ◽

General Pattern ◽

Male Meiosis ◽

Present Knowledge ◽

Microtus Arvalis ◽

Present Contribution ◽

Original Size ◽

Heterogametic Sex

The male has proven to be the heterogametic sex in all mammals studied so far. As is well known, the males usually have the sex chromosomes XY and the females XX. In recent years, however, many exceptions from this general pattern have been discovered. With our present knowledge, the different sex chromosome mechanisms in mammals may be divided into five main groups, and the first of them into subgroups, as follows: (i) Species with XX/XY sex chromosomes: (a) X of original size (see below), Y small; (b) X large, Y small; (c) X large, Y large: (i) end-to-end association of X and Y at male meiosis, (ii) chiasma between X and Y at male meiosis. (ii) Species with XX/XY 1 Y 2 sex chromosomes. (iii) Species with X 1 X 1 X 2 X 2 /X 1 X 2 Y sex chromosomes. (iv) Species with complicated or unknown mechanisms for sex determination. (v) Species with mosaicism of the sex chromosomes, but apparently with an XX/XY mechanism for sex determination. The present contribution will mainly deal with unusual sex chromosome inheritance, that is the groups (ii), (iii) and (iv) above, but the other two groups will also be briefly discussed and examples will be given. Recently Raicu, Kirillova & Hamar (1969) described a new sex chromosome mechanism ( X 1 X 1 X 2 X 2 /X 1 X 2 Y 1 Y 2 ) in the vole Microtus arvalis , but this observation was not confirmed by Schmid (1969), who found an ordinary XX/XY mechanism with both X and Y readily identifiable and of ‘normal’ size, the X comprising 5.6% of ( n A + X) and Y being the smallest chromosome of the complement. Late DNA replication was demonstrated in the allocyclic X and in the Y. Also Wolf (1969) found normal sex chromosomes in this species with no multivalents at male meiosis.

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Genome-wide association mapping uncovers sex-associated copy number variation markers and female hemizygous regions on the W chromosome in Salix viminalis

BMC Genomics ◽

10.1186/s12864-021-08021-2 ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Henrik R. Hallingbäck ◽

Pascal Pucholt ◽

Pär K. Ingvarsson ◽

Ann Christin Rönnberg-Wästljung ◽

Sofia Berlin

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Chromosome 9 ◽

Genome Wide Association ◽

Salix Viminalis ◽

Chromosome 15 ◽

W Chromosome ◽

Genome Wide ◽

Heterogametic Sex

Abstract Background Sex chromosomes are in some species largely undifferentiated (homomorphic) with restricted sex determination regions. Homomorphic but different sex chromosomes are found in the closely related genera Populus and Salix indicating flexible sex determination systems, ideal for studies of processes involved in sex chromosome evolution. We have performed genome-wide association studies of sex and analysed sex chromosomes in a population of 265 wild collected Salix viminalis accessions and studied the sex determining locus. Results A total of 19,592 markers were used in association analyses using both Fisher’s exact tests and a single-marker mixed linear model, which resulted in 48 and 41 sex-associated (SA) markers respectively. Across all 48 SA markers, females were much more often heterozygous than males, which is expected if females were the heterogametic sex. The majority of the SA markers were, based on positions in the S. purpurea genome, located on chromosome 15, previously demonstrated to be the sex chromosome. Interestingly, when mapping the genotyping-by-sequencing sequence tag harbouring the two SA markers with the highest significance to the S. viminalis genomic scaffolds, five regions of very high similarity were found: three on a scaffold that represents a part of chromosome 15, one on a scaffold that represents a part of chromosome 9 and one on a scaffold not anchored to the genome. Based on segregation differences of the alleles at the two marker positions and on differences in PCR amplification between females and males we conclude that females had multiple copies of this DNA fragment (chromosome 9 and 15), whereas males only had one (chromosome 9). We therefore postulate that the female specific sequences have been copied from chromosome 9 and inserted on chromosome 15, subsequently developing into a hemizygous W chromosome linked region. Conclusions Our results support that sex determination in S. viminalis is controlled by one locus on chromosome 15. The segregation patterns observed at the SA markers furthermore confirm that S. viminalis females are the heterogametic sex. We also identified a translocation from chromosome 9 to the W chromosome.

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The Effect of Hybridization on Dosage Compensation in Member Species of the Anopheles gambiae Species Complex

10.1101/327577 ◽

2018 ◽

Author(s):

Kevin C. Deitz ◽

Willem Takken ◽

Michel A. Slotman

Keyword(s):

Sex Determination ◽

Anopheles Gambiae ◽

Y Chromosome ◽

X Chromosome ◽

Dosage Compensation ◽

Sex Chromosomes ◽

Species Complex ◽

F1 Hybrids ◽

Chromosome Gene ◽

Heterogametic Sex

AbstractDosage compensation has evolved in concert with Y-chromosome degeneration in many taxa that exhibit heterogametic sex chromosomes. Dosage compensation overcomes the biological challenge of a "half dose" of X chromosome gene transcripts in the heterogametic sex. The need to equalize gene expression of a hemizygous X with that of autosomes arises from the fact that the X chromosomes retain hundreds of functional genes that are actively transcribed in both sexes and interact with genes expressed on the autosomes. Sex determination and heterogametic sex chromosomes have evolved multiple times in Diptera, and in each case the genetic control of dosage compensation is tightly linked to sex determination. In the Anopheles gambiae species complex (Culicidae), maleness is conferred by the Y-chromosome gene Yob, which despite its conserved role between species is polymorphic in its copy number between them. Previous work demonstrated that male An. gambiae s.s. males exhibit complete dosage compensation in pupal and adult stages. In the present study we have extended this analysis to three sister species in the An. gambiae complex: An. coluzzii, An. arabiensis, and An. quadriannulatus. In addition, we analyzed dosage compensation in bi-directional F1 hybrids between these species to determine if hybridization results in the mis-regulation and disruption of dosage compensation. Our results confirm that dosage compensation operates in the An. gambiae species complex through the hyper-transcription of the male X chromosome. Additionally, dosage compensation in hybrid males does not differ from parental males, indicating that hybridization does not result in the mis-regulation of dosage compensation.

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Proto-sex locus in large yellow croaker provides insights into early evolution of the sex chromosome

10.1101/2020.06.23.166249 ◽

2020 ◽

Author(s):

Zhiyong Wang ◽

Shijun Xiao ◽

Mingyi Cai ◽

Zhaofang Han ◽

Wanbo Li ◽

...

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Draft Genome ◽

Sex Reversal ◽

Large Yellow Croaker ◽

Larimichthys Crocea ◽

Suppressed Recombination ◽

Heterogametic Sex ◽

Sex Locus

AbstractAutosomal origins of heterogametic sex chromosomes have been inferred frequently from suppressed recombination and gene degeneration manifested in incompletely differentiated sex chromosomes. However, the initial transition of an autosome region to a proto-sex locus has been not explored in depth. By assembling and analyzing a chromosome-level draft genome, we found a recent (evolved 0.26 million years ago), highly homologous, and dmrt1 containing sex-determination locus with slightly reduced recombination in large yellow croaker (Larimichthys crocea), a teleost species with genetic sex determination (GSD) and with undifferentiated sex chromosomes. We observed genomic homology and polymorphic segregation of the proto-sex locus between sexes. Expression of dmrt1 showed a stepwise increase in the development of testis, but not in the ovary. We infer that the inception of the proto-sex locus involves a few divergences in nucleotide sequences and slight suppression of recombination in an autosome region. In androgen-induced sex reversal of genetic females, in addition to dmrt1, genes in the conserved dmrt1 cluster, and the rest of the sex determination network were activated. We provided evidence that broad functional links were shared by genetic sex determination and environmental sex reversal.

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Coexistence of Y, W, and Z sex chromosomes in Xenopus tropicalis

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1505291112 ◽

2015 ◽

Vol 112 (34) ◽

pp. E4752-E4761 ◽

Cited By ~ 44

Author(s):

Álvaro S. Roco ◽

Allen W. Olmstead ◽

Sigmund J. Degitz ◽

Tosikazu Amano ◽

Lyle B. Zimmerman ◽

...

Keyword(s):

Sex Chromosomes ◽

Direct Evidence ◽

Sex Chromosome ◽

Xenopus Tropicalis ◽

Relevant Model ◽

Recent Interest ◽

Different Types ◽

Sex Chromosome System ◽

Heterogametic Sex ◽

System Operating

Homomorphic sex chromosomes and rapid turnover of sex-determining genes can complicate establishing the sex chromosome system operating in a given species. This difficulty exists in Xenopus tropicalis, an anuran quickly becoming a relevant model for genetic, genomic, biochemical, and ecotoxicological research. Despite the recent interest attracted by this species, little is known about its sex chromosome system. Direct evidence that females are the heterogametic sex, as in the related species Xenopus laevis, has yet to be presented. Furthermore, X. laevis’ sex-determining gene, DM-W, does not exist in X. tropicalis, and the sex chromosomes in the two species are not homologous. Here we identify X. tropicalis’ sex chromosome system by integrating data from (i) breeding sex-reversed individuals, (ii) gynogenesis, (iii) triploids, and (iv) crosses among several strains. Our results indicate that at least three different types of sex chromosomes exist: Y, W, and Z, observed in YZ, YW, and ZZ males and in ZW and WW females. Because some combinations of parental sex chromosomes produce unisex offspring and other distorted sex ratios, understanding the sex-determination systems in X. tropicalis is critical for developing this flexible animal model for genetics and ecotoxicology.

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Male-specific restriction of recombination frequency in the sex chromosomes of the medaka, Oryzias latipes

Genetics Research ◽

10.1017/s0016672399003754 ◽

1999 ◽

Vol 73 (3) ◽

pp. 225-231 ◽

Cited By ~ 42

Author(s):

MASARU MATSUDA ◽

SAEMI SOTOYAMA ◽

SATOSHI HAMAGUCHI ◽

MITSURU SAKAIZUMI

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Recombination Frequency ◽

Oryzias Latipes ◽

Body Colour ◽

Specific Restriction ◽

Xx Males ◽

Heterogametic Sex ◽

Male Specific

In the medaka, Oryzias latipes, the mechanism of sex determination (XX/XY) can be revealed by genetic crosses using a body-colour gene, though it does not have cytologically recognizable sex chromosomes. The recombination restriction of sex chromosomes in heterogametic (XY) males has been demonstrated. To elucidate whether the recombination is prevented by the heterogamety of the sex chromosomes or by maleness, we examined the recombination frequencies among three loci located on the sex chromosomes (r, SL1 and SL2) in heterogametic males (XY), homogametic males (XX and YY), homogametic females (XX) and heterogametic females (XY). The recombination frequencies between r–SL1 and SL1–SL2 were as follows: 0, 0 (XY males); 0, 1·5 (XX males); 1·6% (YY males; 1·2%, 14·4% (XY females); 0·8%, 21·8% (XX females). These results indicate that the recombination restriction of the sex chromosomes in heterogametic males does not result from heterogametic sex chromosomes, but from maleness. Such sex-chromosome- specific recombination restriction in heterogametic sex may have triggered the differentiation of sex chromosomes in vertebrates.

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Bisection of the X chromosome disrupts the initiation of chromosome silencing during meiosis in Caenorhabditis elegans

Nature Communications ◽

10.1038/s41467-021-24815-0 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Yisrael Rappaport ◽

Hanna Achache ◽

Roni Falk ◽

Omer Murik ◽

Oren Ram ◽

...

Keyword(s):

Caenorhabditis Elegans ◽

Rna Polymerase Ii ◽

X Chromosome ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Transcription Analysis ◽

X Chromosomes ◽

Unique Character ◽

Active Transcription ◽

Heterogametic Sex

AbstractDuring meiosis, gene expression is silenced in aberrantly unsynapsed chromatin and in heterogametic sex chromosomes. Initiation of sex chromosome silencing is disrupted in meiocytes with sex chromosome-autosome translocations. To determine whether this is due to aberrant synapsis or loss of continuity of sex chromosomes, we engineered Caenorhabditis elegans nematodes with non-translocated, bisected X chromosomes. In early meiocytes of mutant males and hermaphrodites, X segments are enriched with euchromatin assembly markers and active RNA polymerase II staining, indicating active transcription. Analysis of RNA-seq data showed that genes from the X chromosome are upregulated in gonads of mutant worms. Contrary to previous models, which predicted that any unsynapsed chromatin is silenced during meiosis, our data indicate that unsynapsed X segments are transcribed. Therefore, our results suggest that sex chromosome chromatin has a unique character that facilitates its meiotic expression when its continuity is lost, regardless of whether or not it is synapsed.

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Cytogenetic Analysis of the Asian Box Turtles of the Genus Cuora (Testudines, Geoemydidae)

Genes ◽

10.3390/genes12020156 ◽

2021 ◽

Vol 12 (2) ◽

pp. 156

Author(s):

Lorenzo Clemente ◽

Sofia Mazzoleni ◽

Eleonora Pensabene ◽

Tomáš Protiva ◽

Philipp Wagner ◽

...

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Wide Distribution ◽

Iucn Red List ◽

Telomeric Repeats ◽

Rdna Loci ◽

Box Turtles ◽

Genotypic Sex Determination ◽

Poorly Differentiated ◽

Almost All

The Asian box turtle genus Cuora currently comprises 13 species with a wide distribution in Southeast Asia, including China and the islands of Indonesia and Philippines. The populations of these species are rapidly declining due to human pressure, including pollution, habitat loss, and harvesting for food consumption. Notably, the IUCN Red List identifies almost all species of the genus Cuora as Endangered (EN) or Critically Endangered (CR). In this study, we explore the karyotypes of 10 Cuora species with conventional (Giemsa staining, C-banding, karyogram reconstruction) and molecular cytogenetic methods (in situ hybridization with probes for rDNA loci and telomeric repeats). Our study reveals a diploid chromosome number of 2n = 52 chromosomes in all studied species, with karyotypes of similar chromosomal morphology. In all examined species, rDNA loci are detected at a single medium-sized chromosome pair and the telomeric repeats are restricted to the expected terminal position across all chromosomes. In contrast to a previous report, sex chromosomes are neither detected in Cuoragalbinifrons nor in any other species. Therefore, we assume that these turtles have either environmental sex determination or genotypic sex determination with poorly differentiated sex chromosomes. The conservation of genome organization could explain the numerous observed cases of interspecific hybridization both within the genus Cuora and across geoemydid turtles.

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