scholarly journals Cytogenetic Evidence for Sex Chromosomes and Karyotype Evolution in Anguimorphan Lizards

Cells ◽  
2021 ◽  
Vol 10 (7) ◽  
pp. 1612
Author(s):  
Barbora Augstenová ◽  
Eleonora Pensabene ◽  
Lukáš Kratochvíl ◽  
Michail Rovatsos

Anguimorphan lizards are a morphologically variable group of squamate reptiles with a wide geographical distribution. In spite of their importance, they have been cytogenetically understudied. Here, we present the results of the cytogenetic examination of 23 species from five anguimorphan families (Anguidae, Helodermatidae, Shinisauridae, Varanidae and Xenosauridae). We applied both conventional (Giemsa staining and C-banding) and molecular cytogenetic methods (fluorescence in situ hybridization with probes for the telomeric motifs and rDNA loci, comparative genome hybridization), intending to describe the karyotypes of previously unstudied species, to uncover the sex determination mode, and to reveal the distribution of variability in cytogenetic characteristics among anguimorphan lizards. We documented that karyotypes are generally quite variable across anguimorphan lineages, with anguids being the most varying. However, the derived chromosome number of 2n = 40 exhibits a notable long-term evolutionary stasis in monitors. Differentiated ZZ/ZW sex chromosomes were documented in monitors and helodermatids, as well as in the anguids Abronia lythrochila, and preliminary also in Celestus warreni and Gerrhonotus liocephalus. Several other anguimorphan species have likely poorly differentiated sex chromosomes, which cannot be detected by the applied cytogenetic methods, although the presence of environmental sex determination cannot be excluded. In addition, we uncovered a rare case of spontaneous triploidy in a fully grown Varanus primordius.

2021 ◽  
pp. 1-6
Author(s):  
Alexander Kostmann ◽  
Lukáš Kratochvíl ◽  
Michail Rovatsos

Squamate reptiles show high diversity in sex determination ranging from environmental sex determination to genotypic sex determination with varying degrees of differentiation of sex chromosomes. Unfortunately, we lack even basic information on sex determination mode in several lineages of squamates, which prevents full understanding of their diversity and evolution of sex determination. One of the reptilian lineages with missing information on sex determination is the family Gerrhosauridae, commonly known as the plated lizards. Several species of gerrhosaurids have been studied in the past by conventional cytogenetic methods, but sex-specific differences were not identified. In this study, we applied both conventional and molecular cytogenetic methods to metaphases from both sexes of the Peters’ keeled plated lizard (Tracheloptychus petersi). We identified accumulations of rDNA loci in a pair of microchromosomes in metaphases from males, but only in a single microchromosome in females. The restriction of the observed heterozygosity to females suggests a putative ZZ/ZW system of sex chromosomes, which represents the first report of sex chromosomes in a gerrhosaurid lizard. The lack of sex-specific signals in all other cytogenetic methods implies that the sex chromosomes of T. petersi are poorly differentiated in sequence content.


Genes ◽  
2019 ◽  
Vol 10 (11) ◽  
pp. 934 ◽  
Author(s):  
Augstenová ◽  
Mazzoleni ◽  
Kostmann ◽  
Altmanová ◽  
Frynta ◽  
...  

Homologous and differentiated ZZ/ZW sex chromosomes (or derived multiple neo-sex chromosomes) were often described in caenophidian snakes, but sex chromosomes were unknown until recently in non-caenophidian snakes. Previous studies revealed that two species of boas (Boa imperator, B. constrictor) and one species of python (Python bivittatus) independently evolved XX/XY sex chromosomes. In addition, heteromorphic ZZ/ZW sex chromosomes were recently revealed in the Madagascar boa (Acrantophis sp. cf. dumerili) and putatively also in the blind snake Myriopholis macrorhyncha. Since the evolution of sex chromosomes in non-caenophidian snakes seems to be more complex than previously thought, we examined ten species of pythons and boas representing the families Boidae, Calabariidae, Candoiidae, Charinidae, Pythonidae, and Sanziniidae by conventional and molecular cytogenetic methods, aiming to reveal their sex chromosomes. Our results show that all examined species do not possess sex-specific differences in their genomes detectable by the applied cytogenetic methods, indicating the presence of poorly differentiated sex chromosomes or even the absence of sex chromosomes. Interestingly, fluorescence in situ hybridization with telomeric repeats revealed extensive distribution of interstitial telomeric repeats in eight species, which are likely a consequence of intra-chromosomal rearrangements.


PeerJ ◽  
2019 ◽  
Vol 7 ◽  
pp. e6241 ◽  
Author(s):  
Sofia Mazzoleni ◽  
Barbora Augstenová ◽  
Lorenzo Clemente ◽  
Markus Auer ◽  
Uwe Fritz ◽  
...  

For a long time, turtles of the family Geoemydidae have been considered exceptional because representatives of this family were thought to possess a wide variety of sex determination systems. In the present study, we cytogenetically studied Geoemyda spengleri and G. japonica and re-examined the putative presence of sex chromosomes in Pangshura smithii. Karyotypes were examined by assessing the occurrence of constitutive heterochromatin, by comparative genome hybridization and in situ hybridization with repetitive motifs, which are often accumulated on differentiated sex chromosomes in reptiles. We found similar karyotypes, similar distributions of constitutive heterochromatin and a similar topology of tested repetitive motifs for all three species. We did not detect differentiated sex chromosomes in any of the species. For P. smithii, a ZZ/ZW sex determination system, with differentiated sex chromosomes, was described more than 40 years ago, but this finding has never been re-examined and was cited in all reviews of sex determination in reptiles. Here, we show that the identification of sex chromosomes in the original report was based on the erroneous pairing of chromosomes in the karyogram, causing over decades an error cascade regarding the inferences derived from the putative existence of female heterogamety in geoemydid turtles.


Genes ◽  
2021 ◽  
Vol 12 (2) ◽  
pp. 156
Author(s):  
Lorenzo Clemente ◽  
Sofia Mazzoleni ◽  
Eleonora Pensabene ◽  
Tomáš Protiva ◽  
Philipp Wagner ◽  
...  

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.


Genes ◽  
2019 ◽  
Vol 10 (12) ◽  
pp. 1020 ◽  
Author(s):  
Rovatsos ◽  
Altmanová ◽  
Augstenová ◽  
Mazzoleni ◽  
Velenský ◽  
...  

Chameleons are well-known, highly distinctive lizards characterized by unique morphological and physiological traits, but their karyotypes and sex determination system have remained poorly studied. We studied karyotypes in six species of Madagascan chameleons of the genus Furcifer by classical (conventional stain, C-banding) and molecular (comparative genomic hybridization, in situ hybridization with rDNA, microsatellite, and telomeric sequences) cytogenetic approaches. In contrast to most sauropsid lineages, the chameleons of the genus Furcifer show chromosomal variability even among closely related species, with diploid chromosome numbers varying from 2n = 22 to 2n = 28. We identified female heterogamety with cytogenetically distinct Z and W sex chromosomes in all studied species. Notably, multiple neo-sex chromosomes in the form Z1Z1Z2Z2/Z1Z2W were uncovered in four species of the genus (F. bifidus, F. verrucosus, F. willsii, and previously studied F. pardalis). Phylogenetic distribution and morphology of sex chromosomes suggest that multiple sex chromosomes, which are generally very rare among vertebrates with female heterogamety, possibly evolved several times within the genus Furcifer. Although acrodontan lizards (chameleons and dragon lizards) demonstrate otherwise notable variability in sex determination, it seems that female heterogamety with differentiated sex chromosomes remained stable in the chameleons of the genus Furcifer for about 30 million years.


Genes ◽  
2020 ◽  
Vol 11 (5) ◽  
pp. 531
Author(s):  
Grzegorz Suwala ◽  
Marie Altmanová ◽  
Sofia Mazzoleni ◽  
Emmanouela Karameta ◽  
Panayiotis Pafilis ◽  
...  

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.


2020 ◽  
Vol 111 (3) ◽  
pp. 307-313 ◽  
Author(s):  
Stuart V Nielsen ◽  
Brendan J Pinto ◽  
Irán Andira Guzmán-Méndez ◽  
Tony Gamble

Abstract Squamate reptiles (lizards, snakes, and amphibians) are an outstanding group for studying sex chromosome evolution—they are old, speciose, geographically widespread, and exhibit myriad sex-determining modes. Yet, the vast majority of squamate species lack heteromorphic sex chromosomes. Cataloging the sex chromosome systems of species lacking easily identifiable, heteromorphic sex chromosomes, therefore, is essential before we are to fully understand the evolution of vertebrate sex chromosomes. Here, we use restriction site-associated DNA sequencing (RADseq) to classify the sex chromosome system of the granite night lizard, Xantusia henshawi. RADseq is an effective alternative to traditional cytogenetic methods for determining a species’ sex chromosome system (i.e., XX/XY or ZZ/ZW), particularly in taxa with non-differentiated sex chromosomes. Although many xantusiid lineages have been karyotyped, none possess heteromorphic sex chromosomes. We identified a ZZ/ZW sex chromosome system in X. henshawi—the first such data for this family. Furthermore, we report that the X. henshawi sex chromosome contains fragments of genes found on Gallus gallus chromosomes 7, 12, and 18 (which are homologous to Anolis carolinensis chromosome 2), the first vertebrate sex chromosomes to utilize this linkage group.


2021 ◽  
Vol 288 (1943) ◽  
pp. 20202139
Author(s):  
Alexander Kostmann ◽  
Lukáš Kratochvíl ◽  
Michail Rovatsos

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.


2021 ◽  
Vol 22 (16) ◽  
pp. 8670
Author(s):  
Alexander Kostmann ◽  
Barbora Augstenová ◽  
Daniel Frynta ◽  
Lukáš Kratochvíl ◽  
Michail Rovatsos

The lizards of the species-rich clade Scincoidea including cordylids, gerrhosaurids, skinks, and xantusiids, show an almost cosmopolitan geographical distribution and a remarkable ecological and morphological divergence. However, previous studies revealed limited variability in cytogenetic traits. The sex determination mode was revealed only in a handful of gerrhosaurid, skink, and xantusiid species, which demonstrated either ZZ/ZW or XX/XY sex chromosomes. In this study, we explored the karyotypes of six species of skinks, two species of cordylids, and one gerrhosaurid. We applied conventional and molecular cytogenetic methods, including C-banding, fluorescence in situ hybridization with probes specific for telomeric motifs and rDNA loci, and comparative genomic hybridization. The diploid chromosome numbers are rather conserved among these species, but the chromosome morphology, the presence of interstitial telomeric sequences, and the topology of rDNA loci vary significantly. Notably, XX/XY sex chromosomes were identified only in Tiliqua scincoides, where, in contrast to the X chromosome, the Y chromosome lacks accumulations of rDNA loci. We confirm that within the lizards of the scincoidean clade, sex chromosomes remained in a generally poor stage of differentiation.


2021 ◽  
Author(s):  
Xiaolan He ◽  
Jorge R. Flores ◽  
Yu Sun ◽  
John L. Bowman

AbstractSexual differentiation in bryophytes occurs in the dominant gametophytic generation. Over half of bryophytes are dioicous, and this pattern in liverworts is even more profound as over 70% of species are dioicous. However, the evolutionary mechanisms leading to the prevalence of dioicy and the shifts of sexual systems between dioicy and monoicy have remained poorly known. These essential factors in reproductive biology are explored here in light of phylogenetics combined with evidence of genomic characterization of sex chromosomes and sex-determination, as well as cytology. Our analyses and discussions on liverworts are focused on: (1) ancestry and shifts in sexuality, (2) evolution of sex chromosomes and maintenance of haploid dioicy, and (3) environmental impact on the evolution of monoicism. We show that the dioicous condition is ancestral in liverworts, and the evolution of sexual systems is both conserved and stable with an ancient origin, but also highly dynamic in certain more recently diverged lineages. We assume that the haploid dioicy maintained in the course of evolution must be linked to the genetically controlled sex-determination, and transition from genetically to developmentally controlled sex determination, the evolution of monoicism, is driven by ephemeral and unstable environments. Monoicy is less stable in the long-term than dioicy, and thus, ultimately, dioicy is selected in liverworts. It is concluded that sexual dimorphism is maintained through a highly dynamic evolutionary process, sex chromosomes bearing distinct set of evolutionary forces that can have large impacts on genome evolution and may also promote speciation.


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