Novel Sex Chromosomes in 3 Cichlid Fishes from Lake Tanganyika

Gammerdinger, William J; Conte, Matthew A.; Sandkam, Benjamin A.; Ziegelbecker, Angelika; Koblmüller, Stephan; Kocher, Thomas D.

doi:10.1093/jhered/esy003

Cited by 31 publications

(59 citation statements)

References 80 publications

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“…This SD system has been maintained for more than 56 My without driving the evolution of highly differentiated sex chromosomes, similar to what was previously described in E. Previous work on cichlid fishes and true frogs suggested that frequent turnovers could keep sex chromosomes undifferentiated 10,11 . It was proposed for these organisms that autosomes that are already hosting genes involved in sex differentiation pathways could be recruited as new sex chromosomes, facilitating turn overs of sex chromosomes and MSD genes 12 .…”

Section: Discussionsupporting

confidence: 76%

“…In mammals and birds, the same sex determination (SD) system has been maintained over a long evolutionary time with conserved master sex determining (MSD) genes on sex chromosomes [3][4][5][6] . In stark contrast, teleost fish display both GSD and environmental sex determination (ESD) 7,8 , and a remarkable evolutionary lability, driven by dynamic and rapid sex chromosome and MSD gene turnovers [9][10][11][12] . These characteristics have made teleosts an attractive model group to study the process of the evolution of sex chromosomes and the turnover of SD systems.…”

Section: Introductionmentioning

confidence: 99%

“…In the past two decades, fueled by advances in genomics tools, a large diversity of MSD genes have been discovered in teleosts, advancing new hypotheses on how the birth of MSD genes, either by allelic diversification or duplication / translocation [9][10][11][12] , can drive sex chromosome turnover in vertebrates. Teleost MSD genes also provided empirical support for the "limited option" hypothesis which states that certain genes known to be implicated in the sex differentiation pathways are more likely to be recruited as new MSD genes [9][10][11]13 . The majority of these recently discovered MSD genes, however, were found in many diverse teleost clades, making it challenging to infer evolutionary patterns and conserved themes in sex chromosomes turnover.…”

Section: Introductionmentioning

confidence: 99%

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The rise and fall of the ancient northern pike master sex determining gene

Pan

Féron

Jouanno

et al. 2020

Preprint

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Sexual reproduction is a ubiquitous basic feature of life and genetic sex determination is thus widespread, at least among eukaryotes. Understanding the remarkable diversity of sex determination mechanisms, however, is limited by the paucity of empirical studies. Here, we traced back the evolution of sex determination in an entire clade of vertebrates and uncovered that the northern pike (Esox lucius) master sex-determining gene initiated from a 65 to 90 million-year-old gene duplication and remained sex-linked on undifferentiated sex chromosomes for at least 56 million years. Contrasting with its ancient origin, we identified several independent species-or population-specific transitions of sex determination mechanisms in this lineage, including an unexpected complete and recent Y-chromosome loss in some North American northern pike populations. These findings highlight the diversity of the evolutionary fates of master sex-determining genes and raise the importance of careful considerations of population demographic history in sex determination studies. Our study also puts forward the hypothesis that occasional sex reversals and genetic bottlenecks provide a nonadaptive explanation for sex determination transitions.

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Section: Discussionsupporting

confidence: 76%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The rise and fall of the ancient northern pike master sex determining gene

Pan

Féron

Jouanno

et al. 2020

Preprint

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“…Here, we found that only a small part (around 220 kb) of the sex chromosome shows differentiation between X and Y chromosome, suggesting that this sex locus encompasses less than 1% of LG24 in E. lucius . Sex chromosome differentiation has been characterized in a few other teleost species, including Chinese tongue sole [32], Japanese medaka [30,54], stickleback [55], Trinidad guppy [56] and a few cichlid species [57,58]. Compared to these examples, we found that the Northern pike displays a very limited region of suppressed recombination between the sex chromosomes.…”

Section: Discussionmentioning

confidence: 76%

Identification of the master sex determining gene in Northern pike (Esox lucius) reveals restricted sex chromosome differentiation

Pan

Féron

Yano

et al. 2019

Preprint

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Teleost fishes, thanks to their rapid evolution of sex determination mechanisms, provide remarkable opportunities to study the formation of sex chromosomes and the mechanisms driving the birth of new master sex determining (MSD) genes. However, the evolutionary interplay between the sex chromosomes and the MSD genes they harbor is rather unexplored. We characterized a male-specific duplicate of the anti-Müllerian hormone (amh) as the MSD gene in Northern Pike (Esox lucius), using genomic and expression evidences as well as by loss-of-function and gain-of-function experiments. Using RAD-Sequencing from a family panel, we identified Linkage Group (LG) 24 as the sex chromosome and positioned the sex locus in its sub-telomeric region. Furthermore, we demonstrated that this MSD originated from an ancient duplication of the autosomal amh gene, which was subsequently translocated to LG24. Using sex-specific pooled genome sequencing and a new male genome sequence assembled using Nanopore long reads, we also characterized the differentiation of the X and Y chromosomes, revealing a small male-specific insertion containing the MSD gene and a limited region with reduced recombination. Our study depicts an unexpected level of limited differentiation within a pair of sex chromosomes harboring an old MSD gene in a wild population of teleost fish, highlights the pivotal role of genes from the amh pathway in sex determination, as well as the importance of gene duplication as a mechanism driving the turnover of sex chromosomes in this clade.Author SummaryIn stark contrast to mammals and birds, teleosts have predominantly homomorphic sex chromosomes and display a high diversity of sex determining genes. Yet, population level knowledge of both the sex chromosome and the master sex determining gene is only available for the Japanese medaka, a model species. Here we identified and provided functional proofs of an old duplicate of anti-Müllerian hormone (Amh), a member of the Tgf-β family, as the male master sex determining gene in the Northern pike, Esox lucius. We found that this duplicate, named amhby (Y-chromosome-specific anti-Müllerian hormone paralog b), was translocated to the sub-telomeric region of the new sex chromosome, and now amhby shows strong sequence divergence as well as substantial expression pattern differences from its autosomal paralog, amha. We assembled a male genome sequence using Nanopore long reads and identified a restricted region of differentiation within the sex chromosome pair in a wild population. Our results provide insight on the conserved players in sex determination pathways, the mechanisms of sex chromosome turnover, and the diversity of levels of differentiation between homomorphic sex chromosomes in teleosts.

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“…Whole genome sequencing techniques are allowing for the rapid discovery of additional cichlid sex chromosomes (Gammerdinger et al 2016;Gammerdinger, Conte, Sandkam, Penman, et al 2018). Several of these novel sex chromosomes involve chromosome fusions (Gammerdinger, Conte, Sandkam, Ziegelbecker, et al 2018). A chromosome fusion is also associated with an XY sex determination system in the riverine species, Astatotilapia burtoni (Roberts et al 2016).…”

Section: Introductionmentioning

confidence: 99%

Evolution of a sex megachromosome

Conte

Clark

Roberts

et al. 2020

Preprint

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AbstractChromosome size and morphology vary within and among species, but little is known about either the proximate or ultimate causes of these differences. Cichlid fish species in the tribe Oreochromini share an unusual megachromosome that is ~3 times longer than any of the other chromosomes. This megachromosome functions as a sex chromosome in some of these species. We explore two hypotheses of how this sex megachromosome may have evolved. The first hypothesis proposes that it developed by the accumulation of repetitive elements as recombination was reduced around a dominant sex-determination locus, as suggested by traditional models of sex chromosome evolution. An alternative hypothesis is that the megachromosome originated via the fusion of an autosome with a highly-repetitive B chromosome, one of which had carried a sex-determination locus. Here we test these hypotheses using comparative analysis of several chromosome-scale cichlid and teleost genomes. We find the megachromosome consists of three distinct regions based on patterns of recombination, gene and transposable element content, and synteny to the ancestral autosome. A WZ sex-determination locus encompasses the last ~105Mbp of the 134Mbp megachromosome and the last 47Mbp of the megachromosome shares no obvious homology to any ancestral chromosome. Comparisons across 69 teleost genomes reveal the megachromosome contains unparalleled amounts of endogenous retroviral elements, immunoglobulin genes, and long non-coding RNAs. Although the origin of this megachromosome remains ambiguous, it has clearly been a focal point of extensive evolutionary genomic conflicts. This megachromosome represents an interesting system for studying sex chromosome evolution and genomic conflicts.

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Novel Sex Chromosomes in 3 Cichlid Fishes from Lake Tanganyika

Cited by 31 publications

References 80 publications

The rise and fall of the ancient northern pike master sex determining gene

The rise and fall of the ancient northern pike master sex determining gene

Identification of the master sex determining gene in Northern pike (Esox lucius) reveals restricted sex chromosome differentiation

Evolution of a sex megachromosome

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