Sexually dimorphic gene expressions in eels: useful markers for early sex assessment in a conservation context

Geffroy, Benjamin; Guilbaud, Florian; Amilhat, Elsa; Beaulaton, Laurent; Vignon, Matthias; Huchet, Emmanuel; Rives, Jacques; Bobe, Julien; Fostier, Alexis; Guiguen, Yann; Bardonnet, Agnès

doi:10.1038/srep34041

Cited by 30 publications

(15 citation statements)

References 65 publications

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“…In fishes with environmental influence on sex determination, i.e ., with either environmental sex determination or environmental sex reversal (environmental factors overruling genetic factors), the primary sex ratio can only be determined at a time when the decisive processes that occur early in development have set the path to the development of testes or ovaries. It is not surprising that at this time, typically during embryogenesis and/or early larval stages (Devlin & Nagahama, 2002), the sexes show sex‐specific gene expression (Geffroy et al ., 2016; Maitre et al ., 2017). At that time, they also show sex‐specific reactions to environmental stress such as, for example, exposure to exogenous sex hormones at ecologically relevant concentrations (Selmoni et al ., 2019).…”

Section: Physiology Of Temperature Effects On Sex Determinationmentioning

confidence: 99%

Effects of global warming on sex ratios in fishes

Geffroy

Wedekind

2020

Journal of Fish Biology

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In fishes, sex is determined by genetics, the environment or an interaction of both. Temperature is among the most important environmental factors that can affect sex determination. As a consequence, changes in temperature at critical developmental stages can induce biases in primary sex ratios in some species. However, early sex ratios can also be biased by sex‐specific tolerances to environmental stresses that may, in some cases, be amplified by changes in water temperature. Sex‐specific reactions to environmental stress have been observed at early larval stages before gonad formation starts. It is therefore necessary to distinguish between temperature effects on sex determination, generally acting through the stress axis or epigenetic mechanisms, and temperature effects on sex‐specific mortality. Both are likely to affect sex ratios and hence population dynamics. Moreover, in cases where temperature effects on sex determination lead to genotype–phenotype mismatches, long‐term effects on population dynamics are possible, for example temperature‐induced masculinization potentially leading to the loss of Y chromosomes or feminization to male‐biased operational sex ratios in future generations. To date, most studies under controlled conditions conclude that if temperature affects sex ratios, elevated temperatures mostly lead to a male bias. The few studies that have been performed on wild populations seem to confirm this general trend. Recent findings suggest that transgenerational plasticity could mitigate the effects of warming on sex ratios in some populations.

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Section: Physiology Of Temperature Effects On Sex Determinationmentioning

confidence: 99%

Effects of global warming on sex ratios in fishes

Geffroy

Wedekind

2020

Journal of Fish Biology

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“…The essentialness of foxr1 was suggested by the wide-ranging presence of this gene in most vertebrates and the retention of a single copy in most teleosts despite multiple whole genome duplication events, but its biological function is still largely unknown. Previous reports have demonstrated the predominant expression of foxr1 mRNA in the ovary of medaka, eel, and tilapia[8,11,13], but in the male germ cells and spermatids in mouse and human[24]. It was further shown to be abundantly expressed in the early cleavage and gastrula stages of Xenopus embryos, but absent in post-gastrula stages due to rapid degradation of its mRNA, indicating that it is a maternally-inherited transcript[25].…”

Section: Discussionmentioning

confidence: 99%

“…Further, foxo3 was shown to be required for ovarian follicular development, and its knockout in mice led to sterility in female mutants due to progressive degeneration of the developing oocytes and lack of ovarian reserve of mature oocytes[10]. foxr1 was also found to have sexually dimorphic expression in eels ( Anguilla anguilla and Monopterus albus ) and marine medaka (O ryzias melastigma ) which was predominately observed in the ovaries[11–13]. However, despite these observational studies, the function of foxr1 in vertebrates especially its role in reproduction remains unclear.…”

Section: Introductionmentioning

confidence: 99%

foxr1is a novel maternal-effect gene in fish that regulates embryonic cell growth viap21andrictor

Cheung

Patinote

Guiguen

et al. 2018

Preprint

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Short Title: foxr1 regulates embryogenesis via p21 and rictor Summary sentence: The foxr1 gene in zebrafish is a novel maternal-effect gene that is required for proper cell division in the earliest stage of embryonic development possibly as a transcriptional factor for cell cycle progression regulators, p21 and rictor. AbstractThe family of forkhead box (Fox) transcription factors regulate gonadogenesis and embryogenesis, but the role of foxr1/foxn5 in reproduction is unknown. Evolution of foxr1 in vertebrates was examined and the gene found to exist in most vertebrates, including mammals, ray-finned fish, amphibians, and sauropsids. By quantitative PCR and RNA-seq, we found that 5 foxr1 had an ovarian-specific expression in zebrafish, a common feature of maternal-effect genes. In addition, it was demonstrated using in situ hybridization that foxr1 was a maternallyinherited transcript that was highly expressed even in early-stage oocytes and accumulated in the developing eggs during oogenesis. We also analyzed the function of foxr1 in female reproduction using a zebrafish CRISPR/Cas9 knockout model. It was observed that embryos from the foxr1-1 0 deficient females had a significantly lower survival rate whereby they either failed to undergo cell division or underwent abnormal division that culminated in growth arrest at around the midblastula transition and early death. These mutant-derived eggs contained a dramatically increased level of p21, a cell cycle inhibitor, and reduced rictor, a component of mTOR and regulator of cell survival, which were in line with the observed growth arrest phenotype. Our study shows for 1 5 the first time that foxr1 is an essential maternal-effect gene and is required for proper cell division and survival via the p21 and mTOR pathways. These novel findings will broaden our knowledge on the functions of specific maternal factors stored in the developing egg and the underlying mechanisms that contribute to reproductive fitness. 3 2 0 3 5genes were expressed in the gonads, and some of these, including foxl2, foxo3, and foxr1, were specific to XX females [8]. foxl2 and its relatives are known to be key players in ovarian differentiation and oogenesis in vertebrates; it is essential for mammalian ovarian maintenance and through knockout experiments, it was demonstrated that foxl2is a critical regulator of sex determination by regulating ovary development and maintenance also in Nile tilapia, medaka, 4 0 and zebrafish [9]. Further, foxo3 was shown to be required for ovarian follicular development, and its knockout in mice led to sterility in female mutants due to progressive degeneration of the 4 developing oocytes and lack of ovarian reserve of mature oocytes [10]. foxr1 was also found to have sexually dimorphic expression in eels (Anguilla anguilla and Monopterus albus) and marine medaka (Oryzias melastigma) which was predominately observed in the ovaries [11][12][13]. 5However, despite these observational studies, the function of foxr1 in vertebrates especially its role in reproductio...

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“…The limited number of attempts at predicting missing size observations or unobserved size-at-age and growth trajectories may also depend on the intrinsic unpredictability of the growth of some organisms. For instance, in species with environmental sexual determination and sexual dimorphism, such as eels [74], or when growth is faster later in life and is strongly determined by the environment (e.g. ocean growth of anadromous salmonids [75]), it may be impossible to accurately predict later portions of the growth trajectory when only observations early in life are available.…”

Section: Prediction Of Growth Trajectoriesmentioning

confidence: 99%

Biological and statistical interpretation of size-at-age, mixed-effects models of growth

Vincenzi¹,

Jeseňsek²,

Crivellì

2020

R. Soc. open sci.

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The differences in life-history traits and processes between organisms living in the same or different populations contribute to their ecological and evolutionary dynamics. We developed mixed-effect model formulations of the popular size-at-age von Bertalanffy and Gompertz growth functions to estimate individual and group variation in body growth, using as a model system four freshwater fish populations, where tagged individuals were sampled for more than 10 years. We used the software Template Model Builder to estimate the parameters of the mixed-effect growth models. Tests on data that were not used to estimate model parameters showed good predictions of individual growth trajectories using the mixed-effects models and starting from one single observation of body size early in life; the best models had R 2 > 0.80 over more than 500 predictions. Estimates of asymptotic size from the Gompertz and von Bertalanffy models were not significantly correlated, but their predictions of size-at-age of individuals were strongly correlated ( r > 0.99), which suggests that choosing between the best models of the two growth functions would have negligible effects on the predictions of size-at-age of individuals. Model results pointed to size ranks that are largely maintained throughout the lifetime of individuals in all populations.

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Sexually dimorphic gene expressions in eels: useful markers for early sex assessment in a conservation context

Cited by 30 publications

References 65 publications

Effects of global warming on sex ratios in fishes

Effects of global warming on sex ratios in fishes

foxr1is a novel maternal-effect gene in fish that regulates embryonic cell growth viap21andrictor

Biological and statistical interpretation of size-at-age, mixed-effects models of growth

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