Most cited article - PubMed ID 33322017
Independent Evolution of Sex Chromosomes in Eublepharid Geckos, A Lineage with Environmental and Genotypic Sex Determination
Chameleons are well-known lizards with unique morphology and physiology, but their sex determination has remained poorly studied. Madagascan chameleons of the genus Furcifer have cytogenetically distinct Z and W sex chromosomes and occasionally Z1Z1Z2Z2/Z1Z2W multiple neo-sex chromosomes. To identify the gene content of their sex chromosomes, we microdissected and sequenced the sex chromosomes of F. oustaleti (ZZ/ZW) and F. pardalis (Z1Z1Z2Z2/Z1Z2W). In addition, we sequenced the genomes of a male and a female of F. lateralis (ZZ/ZW) and F. pardalis and performed a comparative coverage analysis between the sexes. Despite the notable heteromorphy and distinctiveness in heterochromatin content, the Z and W sex chromosomes share approximately 90% of their gene content. This finding demonstrates poor correlation of the degree of differentiation of sex chromosomes at the cytogenetic and gene level. The test of homology based on the comparison of gene copy number variation revealed that female heterogamety with differentiated sex chromosomes remained stable in the genus Furcifer for at least 20 million years. These chameleons co-opted for the role of sex chromosomes the same genomic region as viviparous mammals, lacertids and geckos of the genus Paroedura, which makes these groups excellent model for studies of convergent and divergent evolution of sex chromosomes.
- Keywords
- Chameleons, Homology, Karyotypes, Microdissection, Sex chromosomes, qPCR,
- MeSH
- Lizards * genetics MeSH
- Evolution, Molecular MeSH
- Sex Chromosomes genetics MeSH
- Sex Determination Processes genetics MeSH
- Mammals genetics MeSH
- Base Sequence MeSH
- DNA Copy Number Variations * MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
The classical hypothesis proposes that the lack of recombination on sex chromosomes arises due to selection for linkage between a sex-determining locus and sexually antagonistic loci, primarily facilitated by inversions. However, cessation of recombination on sex chromosomes could be attributed also to neutral processes, connected with other chromosome rearrangements or can reflect sex-specific recombination patterns existing already before sex chromosome differentiation. Three Coleonyx gecko species share a complex X1X1X2X2/X1X2Y system of sex chromosomes evolved via a fusion of the Y chromosome with an autosome. We analyzed synaptonemal complexes and sequenced flow-sorted sex chromosomes to investigate the effect of chromosomal rearrangement on recombination and differentiation of these sex chromosomes. The gecko sex chromosomes evolved from syntenic regions that were also co-opted also for sex chromosomes in other reptiles. We showed that in male geckos, recombination is less prevalent in the proximal regions of chromosomes and is even further drastically reduced around the centromere of the neo-Y chromosome. We highlight that pre-existing recombination patterns and Robertsonian fusions can be responsible for the cessation of recombination on sex chromosomes and that such processes can be largely neutral.
- MeSH
- Y Chromosome genetics MeSH
- Lizards * genetics MeSH
- Sex Chromosomes genetics MeSH
- Cell Movement MeSH
- Recombination, Genetic MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Geckos (Gekkota), the species-rich clade of reptiles with more than 2200 currently recognized species, demonstrate a remarkable variability in diploid chromosome numbers (2n = 16-48) and mode of sex determination. However, only a small fraction of gekkotan species have been studied with cytogenetic methods. Here, we applied both conventional (karyotype reconstruction and C-banding) and molecular (fluorescence in situ hybridization with probes for rDNA loci and telomeric repeats) cytogenetic analyses in seven species of geckos, namely Blaesodactylus boivini, Chondrodactylus laevigatus, Gekko badenii, Gekko cf. lionotum, Hemidactylus sahgali, Homopholis wahlbergii (Gekkonidae) and Ptyodactylus togoensis (Phyllodactylidae), in order to provide further insights into the evolution of karyotypes in geckos. Our analysis revealed the presence of interstitial telomeric repeats in four species, but we were not able to conclude if they are remnants of previous chromosome rearrangements or were formed by an accumulation of telomeric-like satellite motifs. Even though sex chromosomes were previously identified in several species from the genera Hemidactylus and Gekko by cytogenetic and/or genomic methods, they were not detected by us in any examined species. Our examined species either have poorly differentiated sex chromosomes or, possibly, environmental sex determination. Future studies should explore the effect of temperature and conduct genome-wide analyses in order to identify the mode of sex determination in these species.
- Keywords
- C-banding, FISH, Gekkota, heterochromatin, karyotype, rDNA, sex chromosomes, telomeres,
- MeSH
- Genome-Wide Association Study MeSH
- In Situ Hybridization, Fluorescence MeSH
- Lizards * genetics MeSH
- Karyotyping MeSH
- Sex Chromosomes genetics MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Geckos are an excellent group to study the evolution of sex determination, as they possess a remarkable variability ranging from a complete absence of sex chromosomes to highly differentiated sex chromosomes. We explored sex determination in the Madagascar leaf-tail geckos of the genus Uroplatus. The cytogenetic analyses revealed highly heterochromatic W chromosomes in all three examined species (Uroplatus henkeli, U. alluaudi, U. sikorae). The comparative gene coverage analysis between sexes in U. henkeli uncovered an extensive Z-specific region, with a gene content shared with the chicken chromosomes 8, 20, 26 and 28. The genomic region homologous to chicken chromosome 28 has been independently co-opted for the role of sex chromosomes in several vertebrate lineages, including monitors, beaded lizards and monotremes, perhaps because it contains the amh gene, whose homologs were repeatedly recruited as a sex-determining locus. We demonstrate that all tested species of leaf-tail geckos share homologous sex chromosomes despite the differences in shape and size of their W chromosomes, which are not homologous to the sex chromosomes of other closely related genera. The rather old (at least 40 million years), highly differentiated sex chromosomes of Uroplatus geckos can serve as a great system to study the convergence of sex chromosomes evolved from the same genomic region.
- Keywords
- DNA-seq, cytogenetics, evolution, genomics, qPCR, reptiles, sex chromosomes, sex determination,
- MeSH
- Phylogeny MeSH
- Lizards * genetics MeSH
- Sex Chromosomes genetics MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- Madagascar MeSH
Sex chromosomes are a great example of a convergent evolution at the genomic level, having evolved dozens of times just within amniotes. An intriguing question is whether this repeated evolution was random, or whether some ancestral syntenic blocks have significantly higher chance to be co-opted for the role of sex chromosomes owing to their gene content related to gonad development. Here, we summarize current knowledge on the evolutionary history of sex determination and sex chromosomes in amniotes and evaluate the hypothesis of non-random emergence of sex chromosomes. The current data on the origin of sex chromosomes in amniotes suggest that their evolution is indeed non-random. However, this non-random pattern is not very strong, and many syntenic blocks representing putatively independently evolved sex chromosomes are unique. Still, repeatedly co-opted chromosomes are an excellent model system, as independent co-option of the same genomic region for the role of sex chromosome offers a great opportunity for testing evolutionary scenarios on the sex chromosome evolution under the explicit control for the genomic background and gene identity. Future studies should use these systems more to explore the convergent/divergent evolution of sex chromosomes. This article is part of the theme issue 'Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)'.
- Keywords
- amniotes, co-option, sex chromosomes, vertebrates,
- MeSH
- Biological Evolution * MeSH
- Reptiles genetics growth & development MeSH
- Sex Chromosomes genetics MeSH
- Sex Determination Processes * MeSH
- Birds genetics growth & development MeSH
- Mammals genetics growth & development MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Amniotes possess astonishing variability in sex determination ranging from environmental sex determination (ESD) to genotypic sex determination (GSD) with highly differentiated sex chromosomes. Geckos are one of the few amniote groups with substantial variability in sex determination. What makes them special in this respect? We hypothesized that the extraordinary variability of sex determination in geckos can be explained by two alternatives: 1) unusual lability of sex determination, predicting that the current GSD systems were recently formed and are prone to turnovers; and 2) independent transitions from the ancestral ESD to later stable GSD, which assumes that geckos possessed ancestrally ESD, but once sex chromosomes emerged, they remain stable in the long term. Here, based on genomic data, we document that the differentiated ZZ/ZW sex chromosomes evolved within carphodactylid geckos independently from other gekkotan lineages and remained stable in the genera Nephrurus, Underwoodisaurus, and Saltuarius for at least 15 Myr and potentially up to 45 Myr. These results together with evidence for the stability of sex chromosomes in other gekkotan lineages support more our second hypothesis suggesting that geckos do not dramatically differ from the evolutionary transitions in sex determination observed in the majority of the amniote lineages.
- Keywords
- DNA-seq, genomics, qPCR, reptiles, sex chromosomes, sex determination,
- MeSH
- Biological Evolution MeSH
- Phylogeny MeSH
- Lizards * genetics MeSH
- Sex Chromosomes genetics MeSH
- Sex Determination Processes genetics MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Differentiated sex chromosomes are believed to be evolutionarily stable, while poorly differentiated sex chromosomes are considered to be prone to turnovers. With around 1700 currently known species forming ca 15% of reptile species diversity, skinks (family Scincidae) are a very diverse group of squamates known for their large ecological and morphological variability. Skinks generally have poorly differentiated and cytogenetically indistinguishable sex chromosomes, and their sex determination was suggested to be highly variable. Here, we determined X-linked genes in the common sandfish (Scincus scincus) and demonstrate that skinks have shared the same homologous XX/XY sex chromosomes across their wide phylogenetic spectrum for at least 85 million years, approaching the age of the highly differentiated ZZ/ZW sex chromosomes of birds and advanced snakes. Skinks thus demonstrate that even poorly differentiated sex chromosomes can be evolutionarily stable. The conservation of sex chromosomes across skinks allows us to introduce the first molecular sexing method widely applicable in this group.
- Keywords
- genome, molecular sexing, qPCR, sex chromosomes, sex determination, vertebrates,
- MeSH
- Sex Determination Analysis MeSH
- Phylogeny MeSH
- Snakes MeSH
- Lizards * genetics MeSH
- Sex Chromosomes * genetics MeSH
- Sex Determination Processes MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH