Diversity and Convergence of Sex-Determination Mechanisms in Teleost Fish

Annual Review of Animal Biosciences, Journal Year: 2023, Volume and Issue: 12(1), P. 233 - 259

Published: Oct. 20, 2023

Sexual reproduction is prevalent across diverse taxa. However, sex-determination mechanisms are so that even closely related species often differ in systems. Teleost fish a taxonomic group with frequent turnovers of sex-determining and thus provides us great opportunities to investigate the molecular evolutionary underlying turnover Here, we compile recent studies on diversity fish. We demonstrate genes TGF-β signaling pathway frequently used for master (MSD) genes. MSD arise via two main mechanisms, duplication-and-transposition allelic mutations, few exceptions. also temperature influences sex determination many species, those chromosomes, higher temperatures inducing differentiation into males most cases. Finally, review theoretical models discuss what questions remain elusive.

Language: Английский

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A chromosome‐level genome assembly enables the identification of the follicule stimulating hormone receptor as the master sex‐determining gene in the flatfish Solea senegalensis

Molecular Ecology Resources, Journal Year: 2023, Volume and Issue: 23(4), P. 886 - 904

Published: Jan. 1, 2023

Sex determination (SD) shows huge variation among fish and a high evolutionary rate, as illustrated by the Pleuronectiformes (flatfishes). This order is characterized its adaptation to demersal life, compact genomes diversity of SD mechanisms. Here, we assembled Solea senegalensis genome, flatfish great commercial value, into 82 contigs (614 Mb) combining long- short-read sequencing, which were next scaffolded using highly dense genetic map (28,838 markers, 21 linkage groups), representing 98.9% assembly. Further, established correspondence between assembly chromosomes BAC-FISH. Whole genome resequencing six males females enabled identification 41 single nucleotide polymorphism variants in follicle stimulating hormone receptor (fshr) consistent with an XX/XY system. The observed sex association was validated broader independent sample, providing novel molecular sexing tool. fshr gene displayed differential expression male female gonads from 86 days post-fertilization, when gonad still undifferentiated primordium, concomitant activation amh cyp19a1a, testis ovary marker genes, respectively, females. Y-linked allele, included 24 nonsynonymous showed divergent 3D protein structure, overexpressed compared X-linked allele at all stages gonadal differentiation. We hypothesize mechanism hampering action driving toward testis.

Language: Английский

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Master-Key Regulators of Sex Determination in Fish and Other Vertebrates—A Review

International Journal of Molecular Sciences, Journal Year: 2023, Volume and Issue: 24(3), P. 2468 - 2468

Published: Jan. 27, 2023

In vertebrates, mainly single genes with an allele ratio of 1:1 trigger sex-determination (SD), leading to initial equal sex-ratios. Such are designated master-key regulators (MKRs) and frequently associated DNA structural variations, such as copy-number variation null-alleles. Most MKR knowledge comes from fish, especially cichlids, which serve a genetic model for SD. We list 14 MKRs, dmrt1 has been identified in taxonomically distant species birds fish. The identification MKRs known involvement SD, amh fshr, indicates that common network drives illustrate affects estrogen/androgen equilibrium, suggesting may exert over-expression the gene thus form MKR. However, reason why certain factors constitute whereas others do not is unclear. limited number conserved suggests their heterologous sequences could be used targets future searches additional species. Sex-specific mortality, sex reversal, role temperature multigenic SD examined, claiming these phenomena often consequences artificial hybridization. discuss essentiality taxonomic authentication validate purebred origin before searches.

Language: Английский

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Why and how do Y chromosome stop recombining?

Journal of Evolutionary Biology, Journal Year: 2023, Volume and Issue: 36(3), P. 632 - 636

Published: Jan. 22, 2023

Sex chromosomes either carry a factor like the male-determining factors of mammals (Berta et al., 1990) or plant Silene latifolia (Westergaard, 1958), function in balanced sex-determining systems, as Drosophila (Bridges, 1925) and Caenorhabditis elegans (Meyer, 2022). The sex chromosome pairs these several other species include physically extensive fully Y-linked, male-specific, regions ('MSY') that have undergone 'genetic degeneration' lost most genes are carried on X (X-linked then hemizygous males). Similar losses recombination, similar degeneration, occurred evolution with female heterogamety, including birds Lepidoptera, respectively, reviewed by Wang al. (2014) Fraisse (2017). lack recombination is probably not direct consequence carrying genes, having an essential role determination, since unrelated fish small located within recombining (Koyama 2019; Kuhl 2021; Nacif 2022; Reichwald 2015), completely sex-linked some plants smaller than 1 Mb (Akagi 2014; Harkess 2020). These situations can be explained ways, for example they could reflect recent separate sexes, appearance genome region so-called turnover event (Vicoso, 2019). Species whose pair has changes which formerly stopped previously established therefore important, because tell us became suppressed after their locus evolved. first case to discovered was Eutherian mammals. earliest enlargement MSY involved fusion Y chromosome, autosome Marsupials (Waters 2001). This around 115 million years ago (Cortez 2014). Further enlargements caused subsequent suppression events produced 'evolutionary strata' wide differences sequence divergence between Y-X different (Figure 1). Based genetic map estimated females (which represents ancestral order added chromosome), recently near still recombines, pseudo-autosomal region, 'PAR' (Lahn & Page, 1999; Skaletsky 2003). In two evolved strata humans, median synonymous site values 14% 26%, almost high rest (Sayres Makova, 2013). Very varied divergence, perhaps reflecting strata, also seen latifolia, carnation family (Bergero 2007; Papadopulos 2015). threespine stickleback, without fusions any autosomes, shows clear Figure 1b (Peichel 2020), been inferred ZW Neognathous (Wang A may always such (Charlesworth, However, cases when (shrinking PAR changing its boundary region) demand explanation. Several hypotheses proposed. One idea sexually antagonistic polymorphisms become (e.g. male-benefit allele would reduce fitness more likely spread if closely linked one same effects autosomal). Should mutation establish polymorphism, this generates selection closer linkage (Rice, 1987). difficult test because, non-recombining stratum evolved, will present only Y-linked making analysis impossible. Although mutations might detectable from expression sexes at (perhaps higher males), degeneration expected eventually old evolutionary strata. Another approach population genomic evidence show associations alleles (Dagilis Qiu signal found partially it does whether future lead recombination. search alternatives explain ask ruled out. As described below, new ideas Testing predictions 2 below) requires studies newly evolving genomes, becoming possible, using combination sequencing mapping. study S. dioica (closely related hybridize nature homologous XY chromosomes), published Journal Evolutionary Biology (Filatov, 2022), examines stratum. Y- X-linked nevertheless ascertained identifying male-specific variants gene sequences, samples males natural populations. allowed analyses mentioned above showed parts establishment factor. Clear step those seen, numbers unknown, species' genomes large human yet assembled. mapping suggest extremely rate PAR, thus differ mammalian PARs, crossover concentrated very (Rouyer 1986). Some but dioica, suggesting (and dioica; Campos 2016). end studied them detail. 22 were both (they had populations), 20 classified species, 15 appear forming young (much younger youngest ones humans above) suitable testing about suppression. (MSY) gradually expand hinders pairing sequences meiosis (Jeffries 2021). MSY-X should increase distance into 2). slight trend stratum, outgroup vulgaris increases so responsible (HKA tests, correct effect, detected elevated diversity suggests regions). Interestingly, sharply latifolia-specific shared change possibly discontinuous 1b. time makes seem unlikely loss expansion across includes least (probably 500 kb, density 34 genes/Mb). stickleback slightly (Ks), 3% 4%, Again Ks older predicted. true papaya, 2012), consistent chromosomal inversion models propose expansions involving chance inversions prevent set MSY. advantage outweigh fertility disadvantages heterozygotes, production gametes duplications deficiencies crossovers occur paired inversions. version (Jay Olito 2022) proposes prevents deleterious homozygous males. effect strongest highly recessive effects. Accumulation arises fixing population, must rapidly replace (initially arrangement). process works best populations, account observations time-course formation. involved, data distinguish previous one—both predict current boundary. Only few examples coinciding boundaries far discovered. inversions, others done (Lemaitre 2009). cases, (10 IV seven V), formation require genes. (involving 16 genes) papaya 2012). Clearly, detailed helpful. rearrangements, accumulate stops (Charlesworth 1994), third model decrease expression, dosage compensation simultaneously alleles' even before major deterioration coding reverting standard arrangement (Lenormand Roze, Female-biased indeed observed assumed decreased alleles, while increased enough restore predicts bias quickly sex-linkage evolves. Because evolves part process, strongly female-biased many older) sexes. appears opposite way increasing reach level (in double males, significant difference which, expected, little bias). (reviewed Bachtrog, 2008). Genes compensated seems incomplete It interesting already begun studied, well ones, percent. Under polymorphism hypothesis outlined above, expect gene(s) often pattern predicted just described), Overall, model, do fit observations. Filatov's larger supports (using HKA differences), variants. Whether conclusions confirmed once assembly becomes available, valuable how integrated increasingly accessible kinds allow empirical tests this, potentially For instance, compared somatic tissues, over-represented among biased 155 47 one, did relationship genes' positions (Kitano peer review history article available https://publons.com/publon/10.1111/jeb.14137. commentary there no data.

Language: Английский

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The origin, evolution, and translocation of sex chromosomes in Silurus catfish mediated by transposons

BMC Biology, Journal Year: 2025, Volume and Issue: 23(1)

Published: Feb. 21, 2025

Sex chromosome (SC) evolution is a longstanding topic of focus in evolutionary biology. Teleosts often exhibit rapid turnover SCs and sex-determining (SD) genes, alongside diverse range SC differentiation mechanisms. On the basis new chromosome-scale assemblies three Silurus species (S. microdorsalis, S. glanis, lanzhouensis) two outgroup (Pterocryptis cochinchinensis Kryptopterus bicirrhis), along with our previous meridionalis asotus, we traced genus (Siluriformes), following fate known SD gene amhr2y. Phylogenetic analysis showed that amhr2y occurred at least before divergence Pterocryptis, Kryptopterus, lost P. K. bicirrhis. Chr24 has become ancestor five due to duplication-and-translocation amhr2 mediated by LTR transposon. Then, proto Y was formed maintained shared 60 kb male-specific region (MSY) transposable elements (TEs) expansion gathering. Due continuous TEs accumulation, genes other than MSYs have degenerated or been lost, while non-recombinant regions continue expend, forming different sizes (from 320 550 kb). Two events, one homologous left arm right Chr24) nonhomologous Chr5), occurring among were possibly hAT Helitron transposons. Our results on dynamic trajectory amhr2y, MSYs, catfish indicated variability diversity fish confirmed frequent an important way maintain homology low SCs.

Language: Английский

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Characterization of the male-specific region containing the candidate sex-determining gene in Amur catfish (Silurus asotus) using third-generation- and pool-sequencing data

International Journal of Biological Macromolecules, Journal Year: 2023, Volume and Issue: 248, P. 125908 - 125908

Published: July 22, 2023

Language: Английский

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The Cause–Effect Model of Master Sex Determination Gene Acquisition and the Evolution of Sex Chromosomes

International Journal of Molecular Sciences, Journal Year: 2025, Volume and Issue: 26(7), P. 3282 - 3282

Published: April 1, 2025

The canonical model of vertebrate sex chromosome evolution predicts a one-way trend toward degradation. However, most chromosomes in lower vertebrates are homomorphic. Recent progress studies determination has resulted the discovery more than 30 master (MSD) genes, which from teleost fish. An analysis MSD gene acquisition, recombination suppression, and chromosome-specific sequences revealed correlations modes acquisition chromosomes. Sex remain homomorphic with genes acquired by simple mutations, duplications, allelic variations, or neofunctionalization; contrast, they become heteromorphic chromosomal inversion, fusion, fission. There is no suppression carrying gained through mutations. In there extensive inversion. limited transposition translocation. We propose cause-effect that as consequence explains various vertebrates. A key factor determining whether non-homologous regions created during genes. Chromosome inversion creates inversely homologous but directly sequences, lead to retain potential. Over time, recurrent inverted leads formation strata may cause degradation Depending on nature deletions regions, evolve dosage compensation, selective retention haplo-insufficient be used an alternative strategy.

Language: Английский

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Turnover of sex chromosomes in the Lake Tanganyika cichlid tribe Tropheini (Teleostei: Cichlidae)

Scientific Reports, Journal Year: 2024, Volume and Issue: 14(1)

Published: Jan. 30, 2024

Sex chromosome replacement is frequent in many vertebrate clades, including fish, frogs, and lizards. In order to understand the mechanisms responsible for sex turnover early stages of divergence, it necessary study lineages with recently evolved chromosomes. Here we examine evolution a group African cichlid fishes (tribe Tropheini) which began diverge from one another less than 4 MYA. We have evidence previously unknown system, preliminary indications several additional systems not reported this group. find high frequency estimate minimum 14 turnovers tribe. date origin most common determining system tribe (XY-LG5/19) near base two major sub-clades tribe, about 3.4 MY ago. Finally, observe variation size sex-determining region that suggests independent evolutionary strata species shared sex-determination system. Our results illuminate rapid rate Tropheini set stage further studies dynamics

Language: Английский

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The potential regulatory role of the non-coding RNAs in regulating the exogenous estrogen-induced feminization in Takifugu rubripes gonad

Aquatic Toxicology, Journal Year: 2024, Volume and Issue: 273, P. 107022 - 107022

Published: July 14, 2024

Language: Английский

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Long‐read sequencing in ecology and evolution: Understanding how complex genetic and epigenetic variants shape biodiversity

Molecular Ecology, Journal Year: 2023, Volume and Issue: 32(6), P. 1229 - 1235

Published: March 1, 2023

Ten years ago, the journal Molecular Ecology published a “road map” paper that reviewed past achievements in discipline of molecular ecology, identified research challenges and charted way forward (Andrew et al., 2013). That was motivated by symposium organized during First Joint Congress on Evolutionary Biology (Ottawa, July 6–10, 2012). In addition, it occurred heels major inflection point ecology life sciences more broadly: development uptake “next”- or “second”-generation sequencing technologies, which deliver short DNA reads (typically shorter than 400 bp) at very high throughput (e.g., several billion per run; Goodwin 2016). As such, Andrew al. (2013) emphasized promise second-generation for diverse subdisciplines such as phylogeography, landscape genomics, adaptation speciation. Representing just technical advancement, predicted to stimulate rapid conceptual breakthroughs field, especially nonmodel species (Stapley 2010; Tautz 2010). illustrated any recent issue journal, these predictions were accurate. While has enabled important discoveries forefront this technology does not come without limitations, most prominent is read length. Indeed, additional validation, standard cannot be used traverse complex regions genome repetitive elements, duplications, inversions other forms structural change (Goodwin 2016; Huddleston 2014). Consequently, have remained relatively unexplored. Ironically, however, they may also particularly understanding ecological evolutionary processes (Wellenreuther 2019), given their mutation rates Hastings 2009), fact can extremely abundant—often surpassing single nucleotide polymorphisms fold, terms total length affected (1000 Genomes Project Consortium 2015; Mérot 2023). The obtain spanning tens thousands kilobases already available 10 ago (Hayden, 2009; Munroe & Harris, 2010), been developed providers, best-known are Pacific Biosciences (hereafter “PacBio”) Oxford Nanopore Technologies “Nanopore”). Also referred third-generation sequencing, approaches initially complement short-read data Laszlo 2014; Despite potential utility long reads, adoption slow, primarily due error reported initial iterations instruments (Glenn, 2011; Ip 2015). Recent brought about two developments. First, dropped considerably, some cases below 1%, approaching characteristic This improvements chemistry, base-calling algorithms methods post-sequencing correction (Logsdon 2020; Rang 2018). Second, assembling stretches from become McCoy Selvaraj 2013; Zheng Collectively, helping biologists tackle highly dynamic genome, largely inaccessible until few ago. Perhaps clearly, consequential role long-read getting job done publication first complete, telomere-to-telomere human (Nurk 2022), decades after our made (International Human Genome Sequencing Consortium, 2001). Special Issue highlights ways ecologists utilizing information explore roles otherwise loci. 19 articles comprise issue, covering range plant, animal, bacteria virus study systems, grouped into six sections, we summarize below. doing so, goal emphasize key findings each study. We highlight, where possible, will need overcome coming years, before realizes its full potential. conclude summarizing underlying thread Issue: genetic epigenetic variation, while traditionally difficult study, make substantial contribution anticipate that, with continued improvement area only continue grow, shaping downstream biodiversity consequences variants. “Epigenetics” refers heritable changes expression achieved means direct modification sequence (Bossdorf 2008). mechanisms known, including methylation, histone modifications small RNAs, evolution focused because characterized increased stability over generations (Verhoeven Among different types methylated nucleotides, 5-methylcytosine (5mC) received attention, dominant methylation pattern eukaryotes (Goll Bestor, 2005). epigenomic studies indicated differential wide-ranging relevance. For example, broad repatterning known follow hybridization genomic background (Rapp Wendel, well, 5mC variants found associated environmental variables phenotypic metabolic traits plant animal 2008; Hu Barrett, 2017; Rapp 2005; Verhoeven To genome-wide profiles population samples, one treat bisulphite prior step converts unmethylated cytosines uracil, rendering vs. identifiable opinion Issue, Nielsen (2023) how revolutionizing studies, using an example bacteriophages, repertoire eukaryotes. authors discuss advantages PacBio offer detection modifications, technologies eliminate treatment enable de novo base modifications. Aside illustrating state-of-the-art acquisition analysis, identify current limitations profiling develop dedicated analytical tools minimize noise neighbouring implement reference libraries signature advances achieved, much better positioned understand relevance ongoing arms race between bacteriophages (Nielsen Repetitive transposable elements source novelty. Well-known routes reshuffling chromosomal segments involve include ectopic recombination nonhomologous end-joining, lead variety outcomes deletions, fusions (González Petrov, 2012; Huang Rieseberg, 2020). contributions included section, benefit investigations repeat karyotype patterns synteny. karyotype, Burley use characterize large (134-Mbp) neo-sex chromosome blue-faced honeyeater. Results demonstrated originated via fusion autosome ancestral Z chromosome, diversity differentiation. Remarkably, same appear fused convergently songbird lineages, potentially facilitated repeats shared chromosomes (Burley synteny, Ferguson sequence, assemble compare genomes three Eucalyptus species. transposon-rich synteny loss small-scale rearrangements. Their thus generally accepted view maintain syntenic genome. Moreover, results showed sizeable fraction rearrangements contained genes, therefore drive species-rich widely distributed genus. Rather representing obstacle assembly, focus Peona (2023), investigated satellite 24 birds. Using linked catalogued monomer sizes ranging 20 bp 4 kb dynamic. abundance did align models evolution. Specifically, similar among deeply diverged recently result promising future Wierzbicki piRNA (PIWI-interacting RNA) clusters Drosophila. These rich crucial defence against elements. resolved four Drosophila species, contiguous assemblies data. developing framework quantitative dynamics clusters, includes establishing loci, show evolve rapidly, mainly insertion deletion old ones. Remaining expanding taxonomic breadth cluster evolution, well extending analyses larger out, both stand implementation ecology. Long-read broadening toolset management populations, enabling reconstruction gap-free, fast pace (Kardos 2021). allows us re-evaluate previous conclusions drawn at-risk populations based data, origin, levels inbreeding structure sets allow new gained regarding long-term demographic histories fitness 2021; Wold examples genome-scale vulnerable threatened instance, Li, Yang, rely Hi-C takin, bovid herbivore currently listed International Union Conservation Nature (IUCN; high-quality chromosome-level assembly used, along resequencing demonstrate declines effective size million uncover evidence runs homozygosity caused inbreeding. another Yan investigate intraspecific divergence hot-spring snake endemic Qinghai–Tibet Plateau near IUCN. infer divergence, reconstruct history find genes under selection local adaptation. By combining able document assess differentiation lineages system. Being thoroughly catalogue critically answering fundamental questions biology, wild likely respond when confronted challenging novel environments Yeaman 2016), whether why adaptive repeatedly makes modules Jones number answer questions. Xie mangroves cope unique environment: interface land sea. combination mangrove closely related inland contrast mangroves, whole duplications preceded colonization habitats, do detect polyploidization. Rather, attribute expansion. Additionally, lack parallelism gene family consistent intertidal environment Evidence repeated functional found, Wang, (2023). relied tropical poplar, obtained reads. Comparisons five poplar provided convergent environments. Hotaling provide exciting fast-tracking Antarctic eelpout, representative Zoarcidae ray-finned fish genome-sequenced. turn allowed haemoglobin antifreeze which, strong candidates cold water adaptation, arranged duplicated tandem arrays (Hotaling species-specific waters Southern Ocean. A series section illustrate architecture functionally traits. Nacif conduct comprehensive investigation sex-determining region Midas cichlid fish. forward-genetics, Bionano optical mapping, narrow down sex determination system ~100-kb Y harbours partial but complete coding gene: duplicate anti-Mullerian receptor 2 (amhr2Y). Because amhr2Y shown act locus teleost fishes (Nacif 2023), represents candidate probably parallelism. At extreme scale duplication, Zhu biennial alpine sustained rounds duplication. system, detail multi-omics dimorphic cleistogamy. Known evolved across plants, cleistogamy manifested production open (available cross-pollination) closed (self-fertilizing) flowers, thought reproductive assurance (Zhu An revealed consists 70% sequences. integrating experiments probed metabolites, metabolites differentiate flowers. trait, least partially attributed duplication events Finally, Cohen genetics pesticide resistance Colorado potato beetle. trio-binning approach haploid considerably improved contiguity, compared existing pest pangenome all population-scale then exposure. abundant, accounting ~30% highlighting adaptive. Such process time, underline designed variants, additionally exploit layers sequencing. second article Shipilina consider illustrate, simulated empirical haplotype technology, selective sweeps. graph reconstruction, addition mutation, take account ancestry recombination. information, computationally numbers could vastly improve resolution polymorphisms, identifying multiple sweeps occur (Shipilina proceeds diverge, isolation gradually develop. Genomic pairs, particular those pairs diverged, represent dissecting speciation barrier loci (Ravinet 2017). Several papers continuum suppression undertake detailed pair whitefish allopatry starting around 60,000 came back contact roughly 12,000 (Mérot combined Dwarf Normal genotype Whitefish repeat-rich, 60% corresponding interspersed repeats. proportion enriched classes bursts generating early even incipient speciation, Wersebe freshwater crustacean Daphnia. present scan pulex–pulicaria separated 150,000 (Wersebe D. pulicaria complemented hybrids, Contrary expectations, windows restricted genic Zhang in-depth variation isolation, so far implemented natural hybrid zone established Lycaeides butterflies 2.4 secondary 14,000 (Zhang Structural genotyped parental individuals validated cline 562 zone. deletions exhibit largest departures neutral pointing gene-rich inversions, facilitating analysis epigenomes, genomes, harnessed interactions. broadly relevant contexts pathogen control biological communities assembled. paper, van Steenbrugge virulence cyst nematodes, destructive pathogens worldwide. nematodes outgroup. families effectors, proteins secreted manipulate physiology virulence. illuminating diversification effector facilitate nematodes. should subsequent matching host genotypes. Handy composition gut bacterial carpenter bee incipiently social. case, ability full-length 16S amplicons classify significantly resolution, reveal interactions would cryptic. distinct microbiome components might structured processes, geographical microbial transmission, investigation. collection providing needed basic applied topics discipline, being groups organisms organization. collectively hard now properly traversed play critical diversification. context, scales exceed individuals. obtaining essential step, gain replicate assemblies, pangenomes Issue. there improvements. explicitly improving computational efficiency methods, long-range efficiently samples. road map next-generation observational abilities, areas position, cusp accelerated progress technology. With toolkits ecologists, increasingly push limits ever sustains surrounds us. like acknowledge who contributed reviewers evaluated manuscripts, editors Emily Warschefsky Ben Sibbett help throughout. Not applicable.

Language: Английский

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