Heteromorphic Sex Chromosomes and Their DNA Content in Fish: An Insight through Satellite DNA Accumulation in Megaleporinus elongatus

2020 ◽  
Vol 160 (1) ◽  
pp. 38-46 ◽  
Author(s):  
Carolina Crepaldi ◽  
Patricia P. Parise-Maltempi

The repetitive DNA content of fish sex chromosomes provides valuable insights into specificities and patterns of their genetic sex determination systems. In this study, we revealed the genomic satellite DNA (satDNA) content of Megaleporinuselongatus, a Neotropical fish species with Z1Z1Z2Z2/Z1W1Z2W2 multiple sex chromosomes, through high-throughput analysis and graph-based clustering, isolating 68 satDNA families. By physically mapping these sequences in female metaphases, we discovered 15 of the most abundant satDNAs clustered in its chromosomes, 9 of which were found exclusively in the highly heterochromatic W1. This heteromorphic sex chromosome showed the highest amount of satDNA accumulations in this species. The second most abundant family, MelSat02-26, shared FISH signals with the NOR-bearing pair in similar patterns and is linked to the multiple sex chromosome system. Our results demonstrate the diverse satDNA content in M. elongatus, especially in its heteromorphic sex chromosome. Additionally, we highlighted the different accumulation patterns and distribution of these sequences across species by physically mapping these satDNAs in other Anostomidae, Megaleporinusmacrocephalus and Leporinusfriderici (a species without differentiated sex chromosomes).

2020 ◽  
Vol 160 (3) ◽  
pp. 141-147 ◽  
Author(s):  
Marcelo J. da Silva ◽  
Raquel Fogarin Destro ◽  
Thiago Gazoni ◽  
Hideki Narimatsu ◽  
Paulo S. Pereira dos Santos ◽  
...  

Most eukaryotic genomes contain substantial portions of repetitive DNA sequences. These are located primarily in highly compacted heterochromatin and, in many cases, are one of the most abundant components of the sex chromosomes. In this sense, the anuran Proceratophrys boiei represents an interesting model for analyses on repetitive sequences by means of cytogenetic techniques, since it has a karyotype with large blocks of heterochromatin and a ZZ/ZW sex chromosome system. The present study describes, for the first time, families of satellite DNA (satDNA) in the frog P. boiei. Its genome size was estimated at 1.6 Gb, of which 41% correspond to repetitive sequences, including satDNAs, rDNAs, transposable elements, and other elements characterized as non-repetitive. The satDNAs were mapped by FISH in the centromeric and pericentromeric regions of all chromosomes, suggesting a possible involvement of these sequences in centromere function. SatDNAs are also present in the W sex chromosome, occupying the entire heterochromatic area, indicating a probable contribution of this class of repetitive DNA to the differentiation of the sex chromosomes in this species. This study is a valuable contribution to the existing knowledge on repetitive sequences in amphibians. We show the presence of repetitive DNAs, especially satDNAs, in the genome of P. boiei that might be of relevance in genome organization and regulation, setting the stage for a deeper functional genome analysis of Proceratophrys.


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 376 (1833) ◽  
pp. 20200105 ◽  
Author(s):  
Mitsuaki Ogata ◽  
Kazuo Suzuki ◽  
Yoshiaki Yuasa ◽  
Ikuo Miura

Sex chromosomes generally evolve from a homomorphic to heteromorphic state. Once a heteromorphic system is established, the sex chromosome system may remain stable for an extended period. Here, we show the opposite case of sex chromosome evolution from a heteromorphic to a homomorphic system in the Japanese frog Glandirana rugosa. One geographic group, Neo-ZW, has ZZ-ZW type heteromorphic sex chromosomes. We found that its western edge populations, which are geographically close to another West-Japan group with homomorphic sex chromosomes of XX-XY type, showed homozygous genotypes of sex-linked genes in both sexes. Karyologically, no heteromorphic sex chromosomes were identified. Sex-reversal experiments revealed that the males were heterogametic in sex determination. In addition, we identified another similar population around at the southwestern edge of the Neo-ZW group in the Kii Peninsula: the frogs had homomorphic sex chromosomes under male heterogamety, while shared mitochondrial haplotypes with the XY group, which is located in the east and bears heteromorphic sex chromosomes. In conclusion, our study revealed that the heteromorphic sex chromosome systems independently reversed back to or turned over to a homomorphic system around each of the western and southwestern edges of the Neo-ZW group through hybridization with the West-Japan group bearing homomorphic 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)’.


2016 ◽  
Vol 149 (4) ◽  
pp. 282-289 ◽  
Author(s):  
Michail Rovatsos ◽  
Martina Johnson Pokorná ◽  
Marie Altmanová ◽  
Lukáš Kratochvíl

Geckos in general show extensive variability in sex determining systems, but only male heterogamety has been demonstrated in the members of their legless family Pygopodidae. In the pioneering study published more than 45 years ago, multiple sex chromosomes of the type X1X1X2X2/X1X2Y were described in Burton's legless lizard (Lialisburtonis) based on conventional cytogenetic techniques. We conducted cytogenetic analyses including comparative genomic hybridization and fluorescence in situ hybridization (FISH) with selected cytogenetic markers in this species and the previously cytogenetically unstudied Papua snake lizard (Lialis jicari) to better understand the nature of these sex chromosomes and their differentiation. Both species possess male heterogamety with an X1X1X2X2/X1X2Y sex chromosome system; however, the Y and one of the X chromosomes are not small chromosomes as previously reported in L. burtonis, but the largest macrochromosomal pair in the karyotype. The Y chromosomes in both species have large heterochromatic blocks with extensive accumulations of GATA and AC microsatellite motifs. FISH with telomeric probe revealed an exclusively terminal position of telomeric sequences in L. jicari (2n = 42 chromosomes in females), but extensive interstitial signals, potentially remnants of chromosomal fusions, in L.burtonis (2n = 34 in females). Our study shows that even largely differentiated and heteromorphic sex chromosomes might be misidentified by conventional cytogenetic analyses and that the application of more sensitive cytogenetic techniques for the identification of sex chromosomes is beneficial even in the classical examples of multiple sex chromosomes.


2021 ◽  
Vol 12 ◽  
Author(s):  
Carolina Crepaldi ◽  
Emiliano Martí ◽  
Évelin Mariani Gonçalves ◽  
Dardo Andrea Martí ◽  
Patricia Pasquali Parise-Maltempi

Neotropical fishes have highly diversified karyotypic and genomic characteristics and present many diverse sex chromosome systems, with various degrees of sex chromosome differentiation. Knowledge on their sex-specific composition and evolution, however, is still limited. Satellite DNAs (satDNAs) are tandemly repeated sequences with pervasive genomic distribution and distinctive evolutionary pathways, and investigating satDNA content might shed light into how genome architecture is organized in fishes and in their sex chromosomes. The present study investigated the satellitome of Megaleporinus elongatus, a freshwater fish with a proposed Z1Z1Z2Z2/Z1W1Z2W2 multiple sex chromosome system that encompasses a highly heterochromatic and differentiated W1 chromosome. The species satellitome comprises of 140 different satDNA families, including previously isolated sequences and new families found in this study. This diversity is remarkable considering the relatively low proportion that satDNAs generally account for the M. elongatus genome (around only 5%). Differences between the sexes in regards of satDNA content were also evidenced, as these sequences are 14% more abundant in the female genome. The occurrence of sex-biased signatures of satDNA evolution in the species is tightly linked to satellite enrichment associated with W1 in females. Although both sexes share practically all satDNAs, the overall massive amplification of only a few of them accompanied the W1 differentiation. We also investigated the expansion and diversification of the two most abundant satDNAs of M. elongatus, MelSat01-36 and MelSat02-26, both highly amplified sequences in W1 and, in MelSat02-26’s case, also harbored by Z2 and W2 chromosomes. We compared their occurrences in M. elongatus and the sister species M. macrocephalus (with a standard ZW sex chromosome system) and concluded that both satDNAs have led to the formation of highly amplified arrays in both species; however, they formed species-specific organization on female-restricted sex chromosomes. Our results show how satDNA composition is highly diversified in M. elongatus, in which their accumulation is significantly contributing to W1 differentiation and not satDNA diversity per se. Also, the evolutionary behavior of these repeats may be associated with genome plasticity and satDNA variability between the sexes and between closely related species, influencing how seemingly homeologous heteromorphic sex chromosomes undergo independent satDNA evolution.


Genes ◽  
2021 ◽  
Vol 12 (4) ◽  
pp. 483
Author(s):  
Wen-Juan Ma ◽  
Paris Veltsos

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.


Cells ◽  
2021 ◽  
Vol 10 (3) ◽  
pp. 661
Author(s):  
Ikuo Miura ◽  
Foyez Shams ◽  
Si-Min Lin ◽  
Marcelo de Bello Cioffi ◽  
Thomas Liehr ◽  
...  

Translocation between sex-chromosomes and autosomes generates multiple sex-chromosome systems. It happens unexpectedly, and therefore, the evolutionary meaning is not clear. The current study shows a multiple sex chromosome system comprising three different chromosome pairs in a Taiwanese brown frog (Odorrana swinhoana). The male-specific three translocations created a system of six sex-chromosomes, ♂X1Y1X2Y2X3Y3 -♀X1X1X2X2X3X3. It is unique in that the translocations occurred among three out of the six members of potential sex-determining chromosomes, which are known to be involved in sex-chromosome turnover in frogs, and the two out of three include orthologs of the sex-determining genes in mammals, birds and fishes. This rare case suggests sex-specific, nonrandom translocations and thus provides a new viewpoint for the evolutionary meaning of the multiple sex chromosome system.


2006 ◽  
Vol 66 (1b) ◽  
pp. 205-210 ◽  
Author(s):  
G. G. Born ◽  
L. A. C. Bertollo

Specimens of Hoplias malabaricus from Lagoa Carioca, an isolated lake of the Rio Doce State Park (state of Minas Gerais, Brazil), were cytogenetically studied. The diploid number was found to be constant, i.e., 2n = 42 chromosomes, although two karyotypic forms were found: karyotype A, characterized by 22M + 20SM chromosomes, observed only in a male specimen, and karyotype B, characterized by 24M + 16SM + 2ST and 24M + 17SM + 1ST chromosomes in female and male specimens, respectively. This sex difference found in karyotype B is related to an XX/XY sex chromosome system. Another female specimen of H. malabaricus, also carrying karyotype A, had previously been found in the same lake. The available data indicate that two sympatric cytotypes of H. malabaricus exist in the Lagoa Carioca, with cytotype A occurring at a lower frequency and differing from cytotype B by undifferentiated sex chromosomes.


2020 ◽  
Vol 16 (11) ◽  
pp. 20200648
Author(s):  
Nathan W. Anderson ◽  
Carl E. Hjelmen ◽  
Heath Blackmon

Chromosome fusion and fission are primary mechanisms of karyotype evolution. In particular, the fusion of a sex chromosome and an autosome has been proposed as a mechanism to resolve intralocus sexual antagonism. If sexual antagonism is common throughout the genome, we should expect to see an excess of fusions that join sex chromosomes and autosomes. Here, we present a null model that provides the probability of a sex chromosome autosome fusion, assuming all chromosomes have an equal probability of being involved in a fusion. This closed-form expression is applicable to both male and female heterogametic sex chromosome systems and can accommodate unequal proportions of fusions originating in males and females. We find that over 25% of all chromosomal fusions are expected to join a sex chromosome and an autosome whenever the diploid autosome count is fewer than 16, regardless of the sex chromosome system. We also demonstrate the utility of our model by analysing two contrasting empirical datasets: one from Drosophila and one from the jumping spider genus Habronattus . We find that in the case of Habronattus , there is a significant excess of sex chromosome autosome fusions but that in Drosophila there are far fewer sex chromosome autosome fusions than would be expected under our null model.


Cells ◽  
2020 ◽  
Vol 9 (11) ◽  
pp. 2386
Author(s):  
Worapong Singchat ◽  
Syed Farhan Ahmad ◽  
Nararat Laopichienpong ◽  
Aorarat Suntronpong ◽  
Thitipong Panthum ◽  
...  

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.


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