Never Settling Down: Frequent Changes in Sex Chromosomes

Wei, Kevin H.-C.; Barbash, Daniel A.

doi:10.1371/journal.pbio.1002077

Cited by 7 publications

(7 citation statements)

References 25 publications

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“…Different sex-determination systems, such as male heterogametic XX/XY sex chromosomes and female heterogametic ZZ/ZW sex chromosomes, as well as their numerous variants, have been revealed (Bachtrog et al 2014;Mei and Gui 2015). Along with the rapid development of genomics and molecular genetic techniques, labile sex-determination systems and rapid sex chromosome turnovers have been noticed in both animals and plants recently (Bachtrog et al 2014;Chen et al 2014;Cortez et al 2014;Graves 2014;Wei and Barbash 2015). Although how neo-sex chromosomes evolved (Roberts et al 2009;Cortez et al 2014;Vicoso and Bachtrog 2015) and how unisexual and sexual reproduction modes transformed (Jokela et al 2009;Zhang et al 2015) have been revealed, the association between sex chromosome origin and reproduction mode transition from unisexual to sexual reproduction remains unclear in vertebrates.…”

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confidence: 99%

Extra Microchromosomes Play Male Determination Role in Polyploid Gibel Carp

Li¹,

Zhang²,

Zhang³

et al. 2016

Genetics

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Sex is generally determined by sex chromosomes in vertebrates, and sex chromosomes exhibit the most rapidly-evolving traits. Sex chromosome evolution has been revealed previously in numerous cases, but the association between sex chromosome origin and the reproduction mode transition from unisexual to sexual reproduction remains unclear. Here, we have isolated a male-specific sequence via analysis of amplified fragment length polymorphism from polyploid gibel carp (Carassius gibelio), a species that not only has the ability to reproduce unisexually but also contains males in wild populations. Subsequently, we have found through FISH analysis that males have several extra microchromosomes with repetitive sequences and transposable elements when compared to females. Moreover, we produced sex-reversed physiological females with a male-specific marker by using estradiol hormone treatment, and two gynogenetic families were established from them. In addition, the male incidence rates of two gynogenetic families were revealed to be closely associated with the extra microchromosome number of the sex-reversed physiological females. These results suggest that the extra microchromosomes in males might resemble a common feature of sex chromosomes and might play a significant role in male determination during the evolutionary trajectory of the reproduction mode transition from unisexual to sexual reproduction in the polyploid fish.KEYWORDS microchromosome; sex determination; sex chromosome; polyploid; gibel carp; genetics of sex S EX is a common phenomenon in nature and also one of the most important topics in life sciences, especially in evolutionary biology and genetics (Graves 2008). Most vertebrates are gonochoristic and reproduce by sexual reproduction. Different sex-determination systems, such as male heterogametic XX/XY sex chromosomes and female heterogametic ZZ/ZW sex chromosomes, as well as their numerous variants, have been revealed (Bachtrog et al. 2014;Mei and Gui 2015). Along with the rapid development of genomics and molecular genetic techniques, labile sex-determination systems and rapid sex chromosome turnovers have been noticed in both animals and plants recently (Bachtrog et al. 2014;Chen et al. 2014;Cortez et al. 2014;Graves 2014;Wei and Barbash 2015). Although how neo-sex chromosomes evolved (Roberts et al. 2009;Cortez et al. 2014;Vicoso and Bachtrog 2015) and how unisexual and sexual reproduction modes transformed (Jokela et al. 2009;Zhang et al. 2015) have been revealed, the association between sex chromosome origin and reproduction mode transition from unisexual to sexual reproduction remains unclear in vertebrates.The gibel carp, Carassius gibelio, has a wide geographic distribution in the Eurasian continent (Hanfling et al. 2005;Li and Gui 2008;Gui and Zhou 2010;Jakovlic and Gui 2011;Jiang et al. 2013) and diverse gynogenetic strains have been identified using biological traits and genetic markers (Zhou et al. 2000a;Yang and Gui 2004;Guo and Gui 2008). As a hexaploid with .150 chromosomes (...

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confidence: 99%

Extra Microchromosomes Play Male Determination Role in Polyploid Gibel Carp

Li¹,

Zhang²,

Zhang³

et al. 2016

Genetics

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“…In this report, the analysis of Achilles revealed several of its features, such as its abundance and distribution in the olive fly genome or its structural plasticity. Even if the assembly of Y’s protein-coding genes is still a challenge, there are hints supporting the notion that Y heterochromatin may have functional consequences on gene regulation, raising the possibility that variation in heterochromatin, such as copy number of transposable elements and simple-sequence repeats, is under selection [ 76 ]. Therefore the unraveling of the evolutionary history of such elements which integrated into heterochromatin enriched regions, as is the Y chromosome, may ultimately improve the efforts aiming at the manipulation of otherwise intractable regions of the genome.…”

Section: Discussionmentioning

confidence: 99%

Achilles, a New Family of Transcriptionally Active Retrotransposons from the Olive Fruit Fly, with Y Chromosome Preferential Distribution

et al. 2015

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Sex chromosomes have many unusual features relative to autosomes. The in depth exploration of their structure will improve our understanding of their origin and divergence (degeneration) as well as the evolution of genetic sex determination pathways which, most often are attributed to them. In Tephritids, the structure of Y chromosome, where the male-determining factor M is localized, is largely unexplored and limited data concerning its sequence content and evolution are available. In order to get insight into the structure and organization of the Y chromosome of the major olive insect pest, the olive fly Bactrocera oleae, we characterized sequences from a Pulse Field Gel Electrophoresis (PFGE)-isolated Y chromosome. Here, we report the discovery of the first olive fly LTR retrotransposon with increased presence on the Y chromosome. The element belongs to the BEL-Pao superfamily, however, its sequence comparison with the other members of the superfamily suggests that it constitutes a new family that we termed Achilles. Its ~7.5 kb sequence consists of the 5’LTR, the 5’non-coding sequence and the open reading frame (ORF), which encodes the polyprotein Gag-Pol. In situ hybridization to the B. oleae polytene chromosomes showed that Achilles is distributed in discrete bands dispersed on all five autosomes, in all centromeric regions and in the granular heterochromatic network corresponding to the mitotic sex chromosomes. The between sexes comparison revealed a variation in Achilles copy number, with male flies possessing 5–10 copies more than female (CI range: 18–38 and 12–33 copies respectively per genome). The examination of its transcriptional activity demonstrated the presence of at least one intact active copy in the genome, showing a differential level of expression between sexes as well as during embryonic development. The higher expression was detected in male germline tissues (testes). Moreover, the presence of Achilles-like elements in different species of the Tephritidae family suggests an ancient origin of this element.

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“…In both ( c ) and ( d ), the old X may eventually gain diploidy through non-disjunction and subsequently lose dosage compensation, becoming an ordinary autosome pair. Figure adapted from [ 7 ]. Note that although ( c ) and ( d ) are shown as leading to chromosome turnovers, this progression is not inevitable.…”

Section: Sex Chromosome Evolutionmentioning

confidence: 99%

Sex chromosome evolution: historical insights and future perspectives

Abbott

Nordén

Hansson³

2017

Proc. R. Soc. B.

143

129

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Many separate-sexed organisms have sex chromosomes controlling sex determination. Sex chromosomes often have reduced recombination, specialized (frequently sex-specific) gene content, dosage compensation and heteromorphic size. Research on sex determination and sex chromosome evolution has increased over the past decade and is today a very active field. However, some areas within the field have not received as much attention as others. We therefore believe that a historic overview of key findings and empirical discoveries will put current thinking into context and help us better understand where to go next. Here, we present a timeline of important conceptual and analytical models, as well as empirical studies that have advanced the field and changed our understanding of the evolution of sex chromosomes. Finally, we highlight gaps in our knowledge so far and propose some specific areas within the field that we recommend a greater focus on in the future, including the role of ecology in sex chromosome evolution and new multilocus models of sex chromosome divergence.

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Never Settling Down: Frequent Changes in Sex Chromosomes

Abstract: A new study reveals multiple dramatic changes in sex chromosome structure and identity in flies; such transitions are accompanied by a series of genomic events that affect chromosome biology, gene regulation, and sex determination. See the accompanying Research Article.

Cited by 7 publications

References 25 publications

Extra Microchromosomes Play Male Determination Role in Polyploid Gibel Carp

Extra Microchromosomes Play Male Determination Role in Polyploid Gibel Carp

Achilles, a New Family of Transcriptionally Active Retrotransposons from the Olive Fruit Fly, with Y Chromosome Preferential Distribution

Sex chromosome evolution: historical insights and future perspectives

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