Population Consequences of Environmental Sex Reversal

Cotton, Samuel; Wedekind, Claus

doi:10.1111/j.1523-1739.2008.01053.x

Cited by 81 publications

(123 citation statements)

References 40 publications

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“…In the worst scenario, the occasional occurrence of feminizing cold outbreaks (leading to the overabundance of the Y chromosome in the population through the formation of XY females and subsequently of YY supermales) interspersed with masculinizing warm conditions could lead to drastic masculinization and sudden demographic collapse (see e.g. Cotton & Wedekind, 2009). …”

Section: Discussionmentioning

confidence: 99%

“…Sex reversal may occur in natural fish populations of GSD/TSD‐bearing species like pejerrey as a result of climatic events or exposure to endocrine‐disrupting chemicals and cause imbalances in sex ratios (Brown et al., 2015; Cotton & Wedekind, 2009; Strüssmann, Conover, Somoza, & Miranda, 2010). In fact, sex‐reversed pejerrey males and females have previously been detected in a wild population in Lake Kasumigaura (Yamamoto et al., 2014).…”

Section: Introductionmentioning

confidence: 99%

“…Both types of sex reversal in pejerrey appear to be viable and fertile, as for example in this study, and could mate in the wild causing skews in genetic sex ratios such as from the mating of sex‐reversed XX males with normal XX females or sex‐reversed XY females with normal XY males. The latter cross may potentially yield also YY offspring, sometimes called “supermales” because they would yield all‐XY progenies when mating with normal XX females (Cotton & Wedekind, 2009; Wedekind, 2012). …”

Section: Introductionmentioning

confidence: 99%

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Demonstration of viability and fertility and development of a molecular tool to identify YY supermales in a fish with both genotypic and environmental sex determination

Tashiro

Zhang

Kakuta

et al. 2018

Ecology and Evolution

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The pejerrey possesses a genotypic sex determination system driven by the amhy gene and yet shows marked temperature‐dependent sex determination. Sex‐reversed XY females have been found in a naturally breeding population established in Lake Kasumigaura, Japan. These females could mate with normal XY males and generate YY “supermale” individuals that, if viable and fertile, would sire only genotypic male offspring. This study was conducted to verify the viability, gender, and fertility of YY pejerrey and to develop a molecular method for their identification. Production of YY fish was attempted by crossing a thermally sex‐reversed XY female and an XY male, and rearing the progeny until sexual maturation. To identify the presumable YY individuals, we first conducted a PCR analysis using amhy‐specific primers to screen only amhy‐positive (XY and YY) fish. This screening showed that 60.6% of the progeny was amhy‐positive, which suggested the presence of YY fish. We then conducted a second screening by qPCR in order to identify the individuals with two amhy copies in their genome. This screening revealed 13 individuals, all males, with values twice higher than the other 30 amhy‐positive fishes, suggesting they have a YY complement. This assumption as well as the viability, fertility, and “supermale” nature of these individuals was confirmed in progeny tests with XX females that yielded 100% amhy‐positive offspring. These results demonstrate that qPCR can obviate progeny test as a means to identify the genotypic sex and therefore may be useful for the survey of all three possible genotypes in wild populations.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Demonstration of viability and fertility and development of a molecular tool to identify YY supermales in a fish with both genotypic and environmental sex determination

Tashiro

Zhang

Kakuta

et al. 2018

Ecology and Evolution

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“…If they reach adulthood and reproduce, neomales can produce sex-biased (75% females) progeny in a ZZ/ZW system, if the WW genotype is viable (76), or 100% females in a XX/XY system (22). Severely biased sex ratios may have potentially detrimental consequences for population viability (77). Another important question is whether the FHT2 individuals with a masculinized gonadal transcriptome would be able to develop a fully mature gonad or not and, if so, whether they would produce viable germ cells.…”

Section: Discussionmentioning

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.

119

136

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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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“…The prevalence and significance of environmental sex reversal in the wild is therefore still unclear (Wedekind 2010). So far, the consequences of environmentally induced sex reversal have only been analyzed in theoretical studies (Kanaiwa and Harada 2002, Hurley et al 2004, Cotton and Wedekind 2009). These studies suggest that environmentally induced sex reversal can change population growth and population sex ratios in ways that may sometimes be counter-intuitive.…”

Section: What Affects Family Sex Ratios?mentioning

confidence: 99%