Abstract
Global climate is warming rapidly, threatening vertebrates with temperature-dependent sex determination (TSD) by disrupting sex ratios and other traits. Less understood are the effects of increased thermal fluctuations predicted to accompany climate change. Greater fluctuations could accelerate feminization of species that produce females under warmer conditions (further endangering TSD animals), or counter it (reducing extinction risk). Here we use novel experiments exposing eggs of Painted Turtles (Chrysemys picta) to replicated profiles recorded in field nests plus mathematically-modified profiles of similar shape but wider oscillations, and develop a new mathematical model for analysis. We show that broadening fluctuations around naturally male-producing (cooler) profiles feminizes developing embryos, whereas embryos from warmer profiles remain female or die. This occurs presumably because wider oscillations around cooler profiles expose embryos to very low temperatures that inhibit development, and to feminizing temperatures where most embryogenesis accrues. Likewise, embryos incubated under broader fluctuations around warmer profiles experience mostly feminizing temperatures, some dangerously high (which increase mortality), and fewer colder values that are insufficient to induce male development. Therefore, as thermal fluctuations escalate with global warming, the feminization of TSD turtle populations could accelerate, facilitating extinction by demographic collapse. Aggressive global CO2 mitigation scenarios (RCP2.6) could prevent these risks, while intermediate actions (RCP4.5 and RCP6.0 scenarios) yield moderate feminization, highlighting the peril that insufficient reductions of greenhouse gas emissions pose for TSD taxa. If our findings are generalizable, TSD squamates, tuatara, and crocodilians that produce males at warmer temperatures could suffer accelerated masculinization, underscoring the broad taxonomic threats of climate change.
Highlights
Unlike most animals that possess sex chromosomes and whose gonadal development is relatively less sensitive to environmental conditions, the sexual fate of many reptiles and some fish is triggered by the temperatures experienced during development[1,2] (TSD), whereas others have mixed mechanisms of sex determination[3]
Additional sources of thermal variation affect temperature-dependent sex determination (TSD) taxa, such as in sea turtles whose nests may be deep enough to lack daily thermal variation, but which experience fluctuating temperatures associated with precipitation events that are predicted to be altered by climate change[15]
To explain the sex ratios produced by the various thermal treatments used in this study we developed a new mathematical model by calculating the weighted Cumulative Temperature Units for each profile (Fig. 3a,b). wCTUs correspond to the integrated time that embryos were exposed to temperatures above and below the pivotal temperature
Summary
Unlike most animals that possess sex chromosomes and whose gonadal development is relatively less sensitive to environmental conditions, the sexual fate of many reptiles and some fish is triggered by the temperatures experienced during development[1,2] (TSD), whereas others have mixed mechanisms of sex determination[3]. Extinction risk escalates when feminization reaches levels that impair population growth, because extreme male scarcity limits reproduction and sex ratio bias promotes the loss of genetic variation Such extreme feminization resulting from contemporary global warming has already been documented in sea turtle populations exposed to rising average temperatures[9]. Earlier work using simple 12 hr-high/12 hr-low temperature oscillation profiles of increasing amplitude (Fig. 1b) demonstrated that Painted Turtles undergo sex reversal when artificial incubation temperatures diverge significantly from average values that produce exclusively males or females when the temperature is constant[14] This earlier study revealed the unappreciated effect that increased thermal variance may have on sex determination[14], which could have important ecological and evolutionary consequences provided that similar effects were experienced by nests in nature. If applicable to other TSD reptiles, including those that produce males at warmer temperatures, underscore the potentially devastating effect of climate change at a broader taxonomic scale than previously appreciated
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