Multiple Sex-Associated Regions and a Putative Sex Chromosome in Zebrafish Revealed by RAD Mapping and Population Genomics

Anderson, Jennifer; Marí, Adriana Rodríguez; Braasch, Ingo; Amores, Angel; Hohenlohe, Paul A.; Batzel, Peter; Postlethwait, John H.

doi:10.1371/journal.pone.0040701

Cited by 204 publications

(206 citation statements)

References 110 publications

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“…S2). The long arm of Chromosome 4 was late replicating in 28 hpf embryos, which is consistent with previously published cytological data (Daga et al 1996;Sola and Gornung 2001;Anderson et al 2012). To further validate our results, an independent experimental replicate of 28 hpf embryos was generated.…”

Section: Resultssupporting

confidence: 91%

“…Sex chromosomes have not been identified in zebrafish, and the genetic basis for their gender determination is unclear. The existence of a sex-associated region (sar4) on Chr 4q has led to the suggestion that it may be an evolving sex chromosome (Anderson et al 2012;Howe et al 2013). Overall, Chr 4q provides a stunning example of developmentally regulated changes in replication timing that occur during vertebrate development.…”

Section: Replication Timing Parallels Enhancer Activationmentioning

confidence: 99%

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DNA replication timing during development anticipates transcriptional programs and parallels enhancer activation

et al. 2017

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In dividing cells, DNA replication occurs in a precise order, but many questions remain regarding the mechanisms of replication timing establishment and regulation. We now have generated genome-wide, high-resolution replication timing maps throughout zebrafish development. Unexpectedly, in the rapid cell cycles preceding the midblastula transition, a defined timing program was present that predicted the initial wave of zygotic transcription. Replication timing was thereafter progressively and continuously remodeled across the majority of the genome, and epigenetic changes involved in enhancer activation frequently paralleled developmental changes in replication timing. The long arm of Chromosome 4 underwent a dramatic developmentally regulated switch to late replication during gastrulation, reminiscent of mammalian X Chromosome inactivation. This study reveals that replication timing is dynamic and tightly linked to epigenetic and transcriptional changes throughout early zebrafish development. These data provide insight into the regulation and functions of replication timing and will enable further mechanistic studies.

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Section: Resultssupporting

confidence: 91%

Section: Replication Timing Parallels Enhancer Activationmentioning

confidence: 99%

DNA replication timing during development anticipates transcriptional programs and parallels enhancer activation

et al. 2017

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“…These data support the earlier claims that sex determination in domesticated zebrafish is polygenic (30,31,33,51). Then, with the temperature experiments performed in this study, we added an additional level of complexity to this polygenic system by showing different family-by-temperature crossing reaction norms, hence demonstrating the existence of GxE interactions.…”

Section: Discussionsupporting

confidence: 89%

“…Data from most cytogenetic studies (for a review, see ref. 29) and breeding experiments (30,31) indicated the lack of sex chromosomes, pointing to PSD, whereas a hormonal sex reversal experiment (32) and restriction siteassociated DNA (RAD) mapping data from crosses involving wild-type parents pointed toward a ZZ/ZW CSD system (33,34). Eventually, comparative analysis of wild-caught and domesticated lines indicated the presence of sex chromosomes in the former and the apparent loss of the region harboring the sexdetermining gene during the domestication process in the latter (34).…”

mentioning

confidence: 99%

Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes

Ribas

Liew

Díaz

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

109

133

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Understanding environmental influences on sex ratios is important for the study of the evolution of sex-determining mechanisms and for evaluating the effects of global warming and chemical pollution. Fishes exhibit sexual plasticity, but the underlying mechanisms of environmental effects on their reproduction are unclear even in the well-established teleost research model, the zebrafish. Here we established the conditions to study the effects of elevated temperature on zebrafish sex. We showed that sex ratio response to elevated temperature is family-specific and typically leads to masculinization (female-to-male sex reversal), resulting in neomales. These results uncovered genotype-by-environment interactions that support a polygenic sex determination system in domesticated (laboratory) zebrafish. We found that some heat-treated fish had gene expression profiles similar to untreated controls of the same sex, indicating that they were resistant to thermal effects. Further, most neomales had gonadal transcriptomes similar to that of regular males. Strikingly, we discovered heat-treated females that displayed a normal ovarian phenotype but with a "male-like" gonadal transcriptome. Such major transcriptomic reprogramming with preserved organ structure has never been reported. Juveniles were also found to have a male-like transcriptome shortly after exposure to heat. These findings were validated by analyzing the expression of genes and signaling pathways associated with sex differentiation. Our results revealed a lasting thermal effect on zebrafish gonads, suggesting new avenues for detection of functional consequences of elevated temperature in natural fish populations in a global warming scenario.A major paradox in developmental biology is the lack of conservation of sex-determining mechanisms even in closely related taxa (1). Thus, in mammals and birds, sex is genetically canalized by a chromosomal sex determination (CSD) system of male (XX/XY in mammals) or female (ZW/ZZ in birds) heterogamety, driven by the action of a master sex-determining gene: sry in mammals and dmrt1 in birds (1). In contrast, fish sex can be very plastic, with the combination of genetic and environmental influences (2). In addition to fish species with CSD, there are species with polygenic sex determination (PSD), in which sex depends on the combined action of several promale and profemale genetic factors, and species with temperature-dependent sex determination (TSD) (3). Understanding how the environment influences sex ratios in vertebrates is of fundamental importance in the study of the evolution of sex-determining mechanisms (4, 5). It is also of practical relevance in evaluating the effects of climate change and chemical pollution (6, 7).The effects of temperature on gene expression during sex differentiation have been investigated in different teleost species, including the African catfish, Clarias gariepinus (8), European sea bass, Dicentrarchus labrax (9, 10), Japanese flounder, Paralichthys olivaceus (11), pejerrey, Odontesthes...

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“…and under different environmental conditions (69). In contrast, cyp19a1a (and cyp19a1b) plays the pivotal role in the production of estrogen, ultimately controlling sexual phenotype in zebrafish (41) and in all animals exhibiting environmental/temperaturedependent sex determination/differentiation (18).…”

Section: Discussionmentioning

confidence: 99%

Climate change and pollution speed declines in zebrafish populations

Brown

Owen

Peters

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Endocrine disrupting chemicals (EDCs) are potent environmental contaminants, and their effects on wildlife populations could be exacerbated by climate change, especially in species with environmental sex determination. Endangered species may be particularly at risk because inbreeding depression and stochastic fluctuations in male and female numbers are often observed in the small populations that typify these taxa. Here, we assessed the interactive effects of water temperature and EDC exposure on sexual development and population viability of inbred and outbred zebrafish (Danio rerio). Water temperatures adopted were 28°C (current ambient mean spawning temperature) and 33°C (projected for the year 2100). The EDC selected was clotrimazole (at 2 μg/L and 10 μg/L), a widely used antifungal chemical that inhibits a key steroidogenic enzyme [cytochrome P450(CYP19) aromatase] required for estrogen synthesis in vertebrates. Elevated water temperature and clotrimazole exposure independently induced maleskewed sex ratios, and the effects of clotrimazole were greater at the higher temperature. Male sex ratio skews also occurred for the lower clotrimazole exposure concentration at the higher water temperature in inbred fish but not in outbred fish. Population viability analysis showed that population growth rates declined sharply in response to male skews and declines for inbred populations occurred at lower male skews than for outbred populations. These results indicate that elevated temperature associated with climate change can amplify the effects of EDCs and these effects are likely to be most acute in small, inbred populations exhibiting environmental sex determination and/or differentiation.

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Multiple Sex-Associated Regions and a Putative Sex Chromosome in Zebrafish Revealed by RAD Mapping and Population Genomics

Cited by 204 publications

References 110 publications

DNA replication timing during development anticipates transcriptional programs and parallels enhancer activation

DNA replication timing during development anticipates transcriptional programs and parallels enhancer activation

Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes

Climate change and pollution speed declines in zebrafish populations

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