Special Issue "Vertebrate Karyotype Evolution: How Far Have We Come, and Where Are We Going?"

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Population and Evolutionary Genetics and Genomics".

Deadline for manuscript submissions: closed (31 March 2021).

Special Issue Editors

Dr. Michail T Rovatsos
E-Mail Website
Guest Editor
Department of Ecology, Faculty of Science, Charles University, 12800 Prague, Czech Republic
Interests: comparative genomics; cytogenetics; karyotype evolution; molecular genetics; repetitive DNA; sex chromosome evolution; sex determination
Dr. Stuart V. Nielsen
E-Mail Website
Guest Editor
Florida Museum of Natural History, University of Florida, Gainesville, FL, USA
Interests: character evolution; comparative genomics; cytogenetics; phylogenetics; sex chromosome evolution; sex determination

Special Issue Information

Dear Colleagues,

With around 70,000 living species, vertebrates include many commercially important and model species, as well as popular nonmodel species with historically enormous importance in research on any field of biology, including karyotype evolution. The most prominent aspects of karyotype evolution in vertebrates involve the variability in sex chromosomes and sex determination systems, the reconstruction of chromosomal rearrangements, the dynamics of repetitive elements, polyploidization, and genome duplication, just to name a few. Although some vertebrate groups are more well-studied, the advent of modern genetic, cytogenetic, genomic and bioinformatic approaches has offered the opportunity to test long-standing hypotheses in both model and nonmodel taxa and led to a resurgence of interest in previously intractable groups. However, there is still much to be discovered across vertebrates. In this Special Issue, we will assemble both conceptual reviews and case studies that expand our knowledge on the dynamic nature of karyotype evolution in vertebrates, both model and nonmodel, using the latest approaches, tools, and methods.

Dr. Michail T Rovatsos
Dr. Stuart V. Nielsen
Guest Editors

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Keywords

  • chromosomal rearrangements
  • sex chromosomes
  • genome evolution
  • karyotype evolution
  • genomics
  • cytogenetics
  • genetics

Published Papers (12 papers)

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Research

Jump to: Review

Article
Molecular Composition of Heterochromatin and Its Contribution to Chromosome Variation in the Microtus thomasi/Microtus atticus Species Complex
Genes 2021, 12(6), 807; https://doi.org/10.3390/genes12060807 - 25 May 2021
Cited by 1 | Viewed by 656
Abstract
The voles of the Microtus thomasi/M. atticus species complex demonstrate a remarkable variability in diploid chromosomal number (2n = 38–44 chromosomes) and sex chromosome morphology. In the current study, we examined by in situ hybridization the topology of four satellite DNA [...] Read more.
The voles of the Microtus thomasi/M. atticus species complex demonstrate a remarkable variability in diploid chromosomal number (2n = 38–44 chromosomes) and sex chromosome morphology. In the current study, we examined by in situ hybridization the topology of four satellite DNA motifs (Msat-160, Mth-Alu900, Mth-Alu2.2, TTAGGG telomeric sequences) and two transposons (LINE, SINE) on the karyotypes of nine chromosome races (i.e., populations with unique cytogenetic traits) of Microtus thomasi, and two chromosomal races of M. atticus. According to the topology of the repetitive DNA motifs, we were able to identify six types of biarmed chromosomes formed from either Robertsonian or/and tandem fusions. In addition, we identified 14 X chromosome variants and 12 Y chromosome variants, and we were able to reconstruct their evolutionary relations, caused mainly by distinct mechanisms of amplification of repetitive DNA elements, including the telomeric sequences. Our study used the model of the Microtus thomasi/M. atticus species complex to explore how repetitive centromeric content can alter from chromosomal rearrangements and can shape the morphology of sex chromosomes, resulting in extensive inter-species cytogenetic variability. Full article
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Article
Comparative Distribution of Repetitive Sequences in the Karyotypes of Xenopus tropicalis and Xenopus laevis (Anura, Pipidae)
Genes 2021, 12(5), 617; https://doi.org/10.3390/genes12050617 - 21 Apr 2021
Viewed by 367
Abstract
Xenopus laevis and its diploid relative, Xenopus tropicalis, are the most used amphibian models. Their genomes have been sequenced, and they are emerging as model organisms for research into disease mechanisms. Despite the growing knowledge on their genomes based on data obtained [...] Read more.
Xenopus laevis and its diploid relative, Xenopus tropicalis, are the most used amphibian models. Their genomes have been sequenced, and they are emerging as model organisms for research into disease mechanisms. Despite the growing knowledge on their genomes based on data obtained from massive genome sequencing, basic research on repetitive sequences in these species is lacking. This study conducted a comparative analysis of repetitive sequences in X. laevis and X. tropicalis. Genomic in situ hybridization (GISH) and fluorescence in situ hybridization (FISH) with Cot DNA of both species revealed a conserved enrichment of repetitive sequences at the ends of the chromosomes in these Xenopus species. The repeated sequences located on the short arm of chromosome 3 from X. tropicalis were not related to the sequences on the short arm of chromosomes 3L and 3S from X. laevis, although these chromosomes were homoeologous, indicating that these regions evolved independently in these species. Furthermore, all the other repetitive sequences in X. tropicalis and X. laevis may be species-specific, as they were not revealed in cross-species hybridizations. Painting experiments in X. laevis with chromosome 7 from X. tropicalis revealed shared sequences with the short arm of chromosome 3L. These regions could be related by the presence of the nucleolus organizer region (NOR) in both chromosomes, although the region revealed by chromosome painting in the short arm of chromosome 3L in X. laevis did not correspond to 18S + 28S rDNA sequences, as they did not colocalize. The identification of these repeated sequences is of interest as they provide an explanation to some problems already described in the genome assemblies of these species. Furthermore, the distribution of repetitive DNA in the genomes of X. laevis and X. tropicalis might be a valuable marker to assist us in understanding the genome evolution in a group characterized by numerous polyploidization events coupled with hybridizations. Full article
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Article
Sex Chromosome Turnover in Bent-Toed Geckos (Cyrtodactylus)
Genes 2021, 12(1), 116; https://doi.org/10.3390/genes12010116 - 19 Jan 2021
Cited by 1 | Viewed by 837
Abstract
Lizards and snakes (squamates) are known for their varied sex determining systems, and gecko lizards are especially diverse, having evolved sex chromosomes independently multiple times. While sex chromosomes frequently turnover among gecko genera, intrageneric turnovers are known only from Gekko and Hemidactylus. [...] Read more.
Lizards and snakes (squamates) are known for their varied sex determining systems, and gecko lizards are especially diverse, having evolved sex chromosomes independently multiple times. While sex chromosomes frequently turnover among gecko genera, intrageneric turnovers are known only from Gekko and Hemidactylus. Here, we used RADseq to identify sex-specific markers in two species of Burmese bent-toed geckos. We uncovered XX/XY sex chromosomes in Cyrtodactylus chaunghanakwaensis and ZZ/ZW sex chromosomes in Cyrtodactylus pharbaungensis. This is the third instance of intrageneric turnover of sex chromosomes in geckos. Additionally, Cyrtodactylus are closely related to another genus with intrageneric turnover, Hemidactylus. Together, these data suggest that sex chromosome turnover may be common in this clade, setting them apart as exceptionally diverse in a group already known for diverse sex determination systems. Full article
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Article
Highly Rearranged Karyotypes and Multiple Sex Chromosome Systems in Armored Catfishes from the Genus Harttia (Teleostei, Siluriformes)
Genes 2020, 11(11), 1366; https://doi.org/10.3390/genes11111366 - 18 Nov 2020
Viewed by 654
Abstract
Harttia comprises an armored catfish genus endemic to the Neotropical region, including 27 valid species with low dispersion rates that are restricted to small distribution areas. Cytogenetics data point to a wide chromosomal diversity in this genus due to changes that occurred in [...] Read more.
Harttia comprises an armored catfish genus endemic to the Neotropical region, including 27 valid species with low dispersion rates that are restricted to small distribution areas. Cytogenetics data point to a wide chromosomal diversity in this genus due to changes that occurred in isolated populations, with chromosomal fusions and fissions explaining the 2n number variation. In addition, different multiple sex chromosome systems and rDNA loci location are also found in some species. However, several Harttia species and populations remain to be investigated. In this study, Harttia intermontana and two still undescribed species, morphologically identified as Harttia sp. 1 and Harttia sp. 2, were cytogenetically analyzed. Harttia intermontana has 2n = 52 and 2n = 53 chromosomes, while Harttia sp. 1 has 2n = 56 and 2n = 57 chromosomes in females and males, respectively, thus highlighting the occurrence of an XX/XY1Y2 multiple sex chromosome system in both species. Harttia sp. 2 presents 2n = 62 chromosomes for both females and males, with fission events explaining its karyotype diversification. Chromosomal locations of the rDNA sites were also quite different among species, reinforcing that extensive rearrangements had occurred in their karyotype evolution. Comparative genomic hybridization (CGH) experiments among some Harttia species evidenced a shared content of the XY1Y2 sex chromosomes in three of them, thus pointing towards their common origin. Therefore, the comparative analysis among all Harttia species cytogenetically studied thus far allowed us to provide an evolutionary scenario related to the speciation process of this fish group. Full article
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Article
Karyotypic Evolution of Sauropsid Vertebrates Illuminated by Optical and Physical Mapping of the Painted Turtle and Slider Turtle Genomes
Genes 2020, 11(8), 928; https://doi.org/10.3390/genes11080928 - 12 Aug 2020
Cited by 1 | Viewed by 1114
Abstract
Recent sequencing and software enhancements have advanced our understanding of the evolution of genomic structure and function, especially addressing novel evolutionary biology questions. Yet fragmentary turtle genome assemblies remain a challenge to fully decipher the genetic architecture of adaptive evolution. Here, we use [...] Read more.
Recent sequencing and software enhancements have advanced our understanding of the evolution of genomic structure and function, especially addressing novel evolutionary biology questions. Yet fragmentary turtle genome assemblies remain a challenge to fully decipher the genetic architecture of adaptive evolution. Here, we use optical mapping to improve the contiguity of the painted turtle (Chrysemys picta) genome assembly and use de novo fluorescent in situ hybridization (FISH) of bacterial artificial chromosome (BAC) clones, BAC-FISH, to physically map the genomes of the painted and slider turtles (Trachemys scripta elegans). Optical mapping increased C. picta’s N50 by ~242% compared to the previous assembly. Physical mapping permitted anchoring ~45% of the genome assembly, spanning 5544 genes (including 20 genes related to the sex determination network of turtles and vertebrates). BAC-FISH data revealed assembly errors in C. picta and T. s. elegans assemblies, highlighting the importance of molecular cytogenetic data to complement bioinformatic approaches. We also compared C. picta’s anchored scaffolds to the genomes of other chelonians, chicken, lizards, and snake. Results revealed a mostly one-to-one correspondence between chromosomes of painted and slider turtles, and high homology among large syntenic blocks shared with other turtles and sauropsids. Yet, numerous chromosomal rearrangements were also evident across chelonians, between turtles and squamates, and between avian and non-avian reptiles. Full article
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Article
Evidence of Interspecific Chromosomal Diversification in Rainbowfishes (Melanotaeniidae, Teleostei)
Genes 2020, 11(7), 818; https://doi.org/10.3390/genes11070818 - 18 Jul 2020
Cited by 1 | Viewed by 1867
Abstract
Rainbowfishes (Melanotaeniidae) are the largest monophyletic group of freshwater fishes occurring in Australia and New Guinea, with 112 species currently recognised. Despite their high taxonomic diversity, rainbowfishes remain poorly studied from a cytogenetic perspective. Using conventional (Giemsa staining, C banding, chromomycin A3 [...] Read more.
Rainbowfishes (Melanotaeniidae) are the largest monophyletic group of freshwater fishes occurring in Australia and New Guinea, with 112 species currently recognised. Despite their high taxonomic diversity, rainbowfishes remain poorly studied from a cytogenetic perspective. Using conventional (Giemsa staining, C banding, chromomycin A3 staining) and molecular (fluorescence in situ hybridisation with ribosomal DNA (rDNA) and telomeric probes) cytogenetic protocols, karyotypes and associated chromosomal characteristics of five species were examined. We covered all major lineages of this group, namely, Running River rainbowfish Melanotaenia sp., red rainbowfish Glossolepis incisus, threadfin rainbowfish Iriatherina werneri, ornate rainbowfish Rhadinocentrus ornatus, and Cairns rainbowfish Cairnsichthys rhombosomoides. All species had conserved diploid chromosome numbers 2n = 48, but karyotypes differed among species; while Melanotaenia sp., G. incisus, and I. werneri possessed karyotypes composed of exclusively subtelo/acrocentric chromosomes, the karyotype of R. ornatus displayed six pairs of submetacentric and 18 pairs of subtelo/acrocentric chromosomes, while C. rhombosomoides possessed a karyotype composed of four pairs of submetacentric and 20 pairs of subtelo/acrocentric chromosomes. No heteromorphic sex chromosomes were detected using conventional cytogenetic techniques. Our data indicate a conserved 2n in Melanotaeniidae, but morphologically variable karyotypes, rDNA sites, and heterochromatin distributions. Differences were observed especially in taxonomically divergent species, suggesting interspecies chromosome rearrangements. Full article
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Article
Assigning the Sex-Specific Markers via Genotyping-by-Sequencing onto the Y Chromosome for a Torrent Frog Amolops mantzorum
Genes 2020, 11(7), 727; https://doi.org/10.3390/genes11070727 - 30 Jun 2020
Cited by 2 | Viewed by 1454
Abstract
We used a genotyping-by-sequencing (GBS) approach to identify sex-linked markers in a torrent frog (Amolops mantzorum), using 21 male and 19 female wild-caught individuals from the same population. A total of 141 putatively sex-linked markers were screened from 1,015,964 GBS-tags via [...] Read more.
We used a genotyping-by-sequencing (GBS) approach to identify sex-linked markers in a torrent frog (Amolops mantzorum), using 21 male and 19 female wild-caught individuals from the same population. A total of 141 putatively sex-linked markers were screened from 1,015,964 GBS-tags via three approaches, respectively based on sex differences in allele frequencies, sex differences in heterozygosity, and sex-limited occurrence. With validations, 69 sex-linked markers were confirmed, all of which point to male heterogamety. The male specificity of eight sex markers was further verified by PCR amplifications, with a large number of additional individuals covering the whole geographic distribution of the species. Y chromosome (No. 5) was microdissected under a light microscope and amplified by whole-genome amplification, and a draft Y genome was assembled. Of the 69 sex-linked markers, 55 could be mapped to the Y chromosome assembly (i.e., 79.7%). Thus, chromosome 5 could be added as a candidate to the chromosomes that are particularly favored for recruitment in sex-determination in frogs. Three sex-linked markers that mapped onto the Y chromosome were aligned to three different promoter regions of the Rana rugosa CYP19A1 gene, which might be considered as a candidate gene for triggering sex-determination in A. mantzorum. Full article
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Article
Molecular Cytogenetic Characterization of the Sicilian Endemic Pond Turtle Emys trinacris and the Yellow-Bellied Slider Trachemys scripta scripta (Testudines, Emydidae)
Genes 2020, 11(6), 702; https://doi.org/10.3390/genes11060702 - 25 Jun 2020
Cited by 2 | Viewed by 829
Abstract
Turtles, a speciose group consisting of more than 300 species, demonstrate karyotypes with diploid chromosome numbers ranging from 2n = 26 to 2n = 68. However, cytogenetic analyses have been conducted only to 1/3rd of the turtle species, often limited to conventional staining [...] Read more.
Turtles, a speciose group consisting of more than 300 species, demonstrate karyotypes with diploid chromosome numbers ranging from 2n = 26 to 2n = 68. However, cytogenetic analyses have been conducted only to 1/3rd of the turtle species, often limited to conventional staining methods. In order to expand our knowledge of the karyotype evolution in turtles, we examined the topology of the (TTAGGG)n telomeric repeats and the rDNA loci by fluorescence in situ hybridization (FISH) on the karyotypes of two emydids: the Sicilian pond turtle, Emys trinacris, and the yellow-bellied slider, Trachemys scripta scripta (family Emydidae). Furthermore, AT-rich and GC-rich chromosome regions were detected by DAPI and CMA3 stains, respectively. The cytogenetic analysis revealed that telomeric sequences are restricted to the terminal ends of all chromosomes and the rDNA loci are localized in one pair of microchromosomes in both species. The karyotype of the Sicilian endemic E. trinacris with diploid number 2n = 50, consisting of 13 pairs of macrochromosomes and 12 pairs of microchromosomes, is presented here for first time. Our comparative examination revealed similar cytogenetic features in Emys trinacris and the closely related E. orbicularis, as well as to other previously studied emydid species, demonstrating a low rate of karyotype evolution, as chromosomal rearrangements are rather infrequent in this group of turtles. Full article
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Article
Cross-Species BAC Mapping Highlights Conservation of Chromosome Synteny across Dragon Lizards (Squamata: Agamidae)
Genes 2020, 11(6), 698; https://doi.org/10.3390/genes11060698 - 25 Jun 2020
Cited by 3 | Viewed by 1264
Abstract
Dragon lizards (Squamata: Agamidae) comprise about 520 species in six subfamilies distributed across Asia, Australasia and Africa. Only five species are known to have sex chromosomes. All of them possess ZZ/ZW sex chromosomes, which are microchromosomes in four species from the subfamily Amphibolurinae, [...] Read more.
Dragon lizards (Squamata: Agamidae) comprise about 520 species in six subfamilies distributed across Asia, Australasia and Africa. Only five species are known to have sex chromosomes. All of them possess ZZ/ZW sex chromosomes, which are microchromosomes in four species from the subfamily Amphibolurinae, but much larger in Phrynocephalus vlangalii from the subfamily Agaminae. In most previous studies of these sex chromosomes, the focus has been on Australian species from the subfamily Amphibolurinae, but only the sex chromosomes of the Australian central bearded dragon (Pogona vitticeps) are well-characterized cytogenetically. To determine the level of synteny of the sex chromosomes of P. vitticeps across agamid subfamilies, we performed cross-species two-colour FISH using two bacterial artificial chromosome (BAC) clones from the pseudo-autosomal regions of P. vitticeps. We mapped these two BACs across representative species from all six subfamilies as well as two species of chameleons, the sister group to agamids. We found that one of these BAC sequences is conserved in macrochromosomes and the other in microchromosomes across the agamid lineages. However, within the Amphibolurinae, there is evidence of multiple chromosomal rearrangements with one of the BACs mapping to the second-largest chromosome pair and to the microchromosomes in multiple species including the sex chromosomes of P. vitticeps. Intriguingly, no hybridization signal was observed in chameleons for either of these BACs, suggesting a likely agamid origin of these sequences. Our study shows lineage-specific evolution of sequences/syntenic blocks and successive rearrangements and reveals a complex history of sequences leading to their association with important biological processes such as the evolution of sex chromosomes and sex determination. Full article
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Article
Interstitial Telomeric Repeats Are Rare in Turtles
Genes 2020, 11(6), 657; https://doi.org/10.3390/genes11060657 - 16 Jun 2020
Cited by 5 | Viewed by 1131
Abstract
Telomeres are nucleoprotein complexes protecting chromosome ends in most eukaryotic organisms. In addition to chromosome ends, telomeric-like motifs can be accumulated in centromeric, pericentromeric and intermediate (i.e., between centromeres and telomeres) positions as so-called interstitial telomeric repeats (ITRs). We mapped the distribution of [...] Read more.
Telomeres are nucleoprotein complexes protecting chromosome ends in most eukaryotic organisms. In addition to chromosome ends, telomeric-like motifs can be accumulated in centromeric, pericentromeric and intermediate (i.e., between centromeres and telomeres) positions as so-called interstitial telomeric repeats (ITRs). We mapped the distribution of (TTAGGG)n repeats in the karyotypes of 30 species from nine families of turtles using fluorescence in situ hybridization. All examined species showed the expected terminal topology of telomeric motifs at the edges of chromosomes. We detected ITRs in only five species from three families. Combining our and literature data, we inferred seven independent origins of ITRs among turtles. ITRs occurred in turtles in centromeric positions, often in several chromosomal pairs, in a given species. Their distribution does not correspond directly to interchromosomal rearrangements. Our findings support that centromeres and non-recombining parts of sex chromosomes are very dynamic genomic regions, even in turtles, a group generally thought to be slowly evolving. However, in contrast to squamate reptiles (lizards and snakes), where ITRs were found in more than half of the examined species, and birds, the presence of ITRs is generally rare in turtles, which agrees with the expected low rates of chromosomal rearrangements and rather slow karyotype evolution in this group. Full article
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Article
Cytogenetic Characterization of Seven Novel satDNA Markers in Two Species of Spined Loaches (Cobitis) and Their Clonal Hybrids
Genes 2020, 11(6), 617; https://doi.org/10.3390/genes11060617 - 04 Jun 2020
Cited by 1 | Viewed by 1047
Abstract
Interspecific hybridization is a powerful evolutionary force. However, the investigation of hybrids requires the application of methodologies that provide efficient and indubitable identification of both parental subgenomes in hybrid individuals. Repetitive DNA, and especially the satellite DNA sequences (satDNA), can rapidly diverge even [...] Read more.
Interspecific hybridization is a powerful evolutionary force. However, the investigation of hybrids requires the application of methodologies that provide efficient and indubitable identification of both parental subgenomes in hybrid individuals. Repetitive DNA, and especially the satellite DNA sequences (satDNA), can rapidly diverge even between closely related species, hence providing a useful tool for cytogenetic investigations of hybrids. Recent progress in whole-genome sequencing (WGS) offers unprecedented possibilities for the development of new tools for species determination, including identification of species-specific satDNA markers. In this study, we focused on spined loaches (Cobitis, Teleostei), a group of fishes with frequent interspecific hybridization. Using the WGS of one species, C. elongatoides, we identified seven satDNA markers, which were mapped by fluorescence in situ hybridization on mitotic and lampbrush chromosomes of C. elongatoides, C. taenia and their triploid hybrids (C. elongatoides × 2C. taenia). Two of these markers were chromosome-specific in both species, one had centromeric localization in multiple chromosomes and four had variable patterns between tested species. Our study provided a novel set of cytogenetic markers for Cobitis species and demonstrated that NGS-based development of satDNA cytogenetic markers may provide a very efficient and easy tool for the investigation of hybrid genomes, cell ploidy, and karyotype evolution. Full article
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Review

Jump to: Research

Review
The Diversity and Evolution of Sex Chromosomes in Frogs
Genes 2021, 12(4), 483; https://doi.org/10.3390/genes12040483 - 26 Mar 2021
Viewed by 1072
Abstract
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 [...] Read more.
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. Full article
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