Warmer waters masculinize wild populations of a fish with temperature-dependent sex determination

Honeycutt, Jamie L.; Deck, Courtney A.; Miller, SB; Severance, M. E.; Atkins, E. B.; Luckenbach, J. Adam; Buckel, Jeffrey A.; Daniels, Harry V.; Rice, James A.; Borski, Russell J.; Godwin, John

doi:10.1038/s41598-019-42944-x

Cited by 50 publications

(45 citation statements)

References 40 publications

(68 reference statements)

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“…Studies of TSD species suggest the answer to both questions is yes. Variation in sex ratio is correlated with nest or water temperatures in nature in crocodilians, lizards, turtles, and fish (Janzen, 1994;Weisrock and Janzen, 1999;Wapstra et al, 2009;Simoncini et al, 2014;Pezaro et al, 2016;Jensen et al, 2018;Patricio et al, 2018;Honeycutt et al, 2019;Mitchell and Janzen, 2019;Tilley et al, 2019). These studies indicate that TSD is operative in nature.…”

Section: Temperature Effects On Development Plasticity In Light Of Glmentioning

confidence: 71%

Embryonic Temperature Programs Phenotype in Reptiles

2020

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Reptiles are critically affected by temperature throughout their lifespan, but especially so during early development. Temperature-induced changes in phenotype are a specific example of a broader phenomenon called phenotypic plasticity in which a single individual is able to develop different phenotypes when exposed to different environments. With climate change occurring at an unprecedented rate, it is important to study temperature effects on reptiles. For example, the potential impact of global warming is especially pronounced in species with temperature-dependent sex determination (TSD) because temperature has a direct effect on a key phenotypic (sex) and demographic (population sex ratios) trait. Reptiles with TSD also serve as models for studying temperature effects on the development of other traits that display continuous variation. Temperature directly influences metabolic and developmental rate of embryos and can have permanent effects on phenotype that last beyond the embryonic period. For instance, incubation temperature programs post-hatching hormone production and growth physiology, which can profoundly influence fitness. Here, we review current knowledge of temperature effects on phenotypic and developmental plasticity in reptiles. First, we examine the direct effect of temperature on biophysical processes, the concept of thermal performance curves, and the process of thermal acclimation. After discussing these reversible temperature effects, we focus the bulk of the review on developmental programming of phenotype by temperature during embryogenesis (i.e., permanent developmental effects). We focus on oviparous species because eggs are especially susceptible to changes in ambient temperature. We then discuss recent work probing the role of epigenetic mechanisms in mediating temperature effects on phenotype. Based on phenotypic effects of temperature, we return to the potential impact of global warming on reptiles. Finally, we highlight key areas for future research, including the identification of temperature sensors and assessment of genetic variation for thermosensitivity.

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Section: Temperature Effects On Development Plasticity In Light Of Glmentioning

confidence: 71%

Embryonic Temperature Programs Phenotype in Reptiles

2020

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“…More broadly, a better understanding of ESD is increasingly important for assessing the biological impacts of climate change on environmentally sensitive species (Parmesan & Yohe, ; Umina et al ., ; Etterson et al ., ; Sinervo, ; IPCC, ). Already populations of ESD species are experiencing skewed sex ratios caused by rising global temperatures (Mitchell & Janzen, ; Refsnider & Janzen, ; Bókony et al ., ; Hays et al ., ; Honeycutt et al ., ). By understanding how an environmental signal is transduced to a sexual outcome, novel conservation management strategies could be devised to avoid or mitigate these impacts of climate change.…”

Section: Applying the Care Model In Theory And Practicementioning

confidence: 97%

Cellular calcium and redox regulation: the mediator of vertebrate environmental sex determination?

et al. 2020

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Many reptiles and some fish determine offspring sex by environmental cues such as incubation temperature. The mechanism by which environmental signals are captured and transduced into specific sexual phenotypes has remained unexplained for over 50 years. Indeed, environmental sex determination (ESD) has been viewed as an intractable problem because sex determination is influenced by a myriad of genes that may be subject to environmental influence. Recent demonstrations of ancient, conserved epigenetic processes in the regulatory response to environmental cues suggest that the mechanisms of ESD have a previously unsuspected level of commonality, but the proximal sensor of temperature that ultimately gives rise to one sexual phenotype or the other remains unidentified. Here, we propose that in ESD species, environmental cues are sensed by the cell through highly conserved ancestral elements of calcium and redox (CaRe) status, then transduced to activate ubiquitous signal transduction pathways, or influence epigenetic processes, ultimately to drive the differential expression of sex genes. The early evolutionary origins of CaRe regulation, and its essential role in eukaryotic cell function, gives CaRe a propensity to be independently recruited for diverse roles as a 'cellular sensor' of environmental conditions. Our synthesis provides the first cohesive mechanistic model connecting environmental signals and sex determination pathways in vertebrates, providing direction and a framework for developing targeted experimentation.

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“…Most studies on temperature effects on sex ratio have been performed under laboratory conditions. A recent study on the southern flounder Paralichthys lethostigma Jordan & Gilbert 1884 combined laboratory experiments with field observations (Honeycutt et al ., 2019). This is a species where temperature extremes (warm and cold) had previously been reported to induce masculinization (Luckenbach et al ., 2003) (C2 in Figure 2).…”

Section: Types Of Temperature Effects On Sex Determinationmentioning

confidence: 99%

“…(2019) used gonadal expression of sex‐specific markers to determine the phenotypic sex of juveniles caught at different locations along the east coast of North Carolina (USA) and observed increasingly male‐biased sex ratios with increasing water temperatures. These temperature effects were then largely confirmed under controlled conditions in the laboratory (Honeycutt et al ., 2019). In another study system, however, laboratory experiments by Pompini et al .…”

Section: Types 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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Warmer waters masculinize wild populations of a fish with temperature-dependent sex determination

Cited by 50 publications

References 40 publications

Embryonic Temperature Programs Phenotype in Reptiles

Embryonic Temperature Programs Phenotype in Reptiles

Cellular calcium and redox regulation: the mediator of vertebrate environmental sex determination?

Effects of global warming on sex ratios in fishes

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