The Lesser Known Challenge of Climate Change: Thermal Variance and Sex-Reversal in Vertebrates with Temperature-Dependent Sex Determination

Abstract

Climate change is expected to disrupt biological systems. Particularly susceptible are species with temperature-dependent sex determination (TSD), as in many reptiles. While the potentially devastating effect of rising mean temperatures on sex ratios in TSD species is appreciated, the consequences of increased thermal variance predicted to accompany climate change remain obscure. Surprisingly, no study has tested if the effect of thermal variance around high-temperatures (which are particularly relevant given climate change predictions) has the same or opposite effects as around lower temperatures. Here we show that sex ratios of the painted turtle (Chrysemys picta) were reversed as fluctuations increased around low and high unisexual mean-temperatures. Unexpectedly, the developmental and sexual responses around female-producing temperatures were decoupled in a more complex manner than around male-producing values. Our novel observations are not fully explained by existing ecological models of development and sex determination, and provide strong evidence that thermal fluctuations are critical for shaping the biological outcomes of climate change.

Molecular Cytogenetic Search for Cryptic Sex Chromosomes in Painted Turtles <b><i>Chrysemys picta</i></b>

“…Balanced sex ratios induce a greater effective population size, a higher population growth potential, and a reduced rate of loss of genetic variation than biased sex ratios. Contrastingly, ESD can drastically bias sex ratios potentially challenging population survival, as for TSD species under climate change [Neuwald and Valenzuela, 2011]. Further, chromosomal sex determination favors the ac- Fig.…”

Ecotoxicological Perspectives of Sex Determination

“…The duration of the thermosensitive period may vary by species, by temperature, and even by population [Yntema, 1979;Pieau and Dorizzi, 1981;Wibbels et al, 1991;Valenzuela, 2001;Hewavisenthi and Parmenter, 2002;Bonach et al, 2011;Rhen et al, 2015]. Under fluctuating temperature regimes, as occur in natural nests, sex is determined by the cumulative effect of the temperatures above the pivotal temperature (or above the value that causes development to halt) experienced during the thermosensitive period Neuwald and Valenzuela, 2011].…”

“…Such changes may be natural as with the climatic changes that the earth has undergone over geological time and which may have mediated transitions in sex determination in turtles [Valenzuela and Adams, 2011]. Other changes are anthropogenic and encompass contemporary climate changes which could endanger many TSD species [Janzen, 1994;Neuwald and Valenzuela, 2011] or habitat degradation from chemical pollution that could alter sex determination by disrupting the genetic machinery responsible for gonadal formation [Hayes et al, 2002]. For instance, soil and water contamination by pesticides and other contaminants from agriculture, industry, and domestic effluents may directly affect the embryonic development of many species of reptiles and amphibians.…”

Regional warming and the thermal regimes of American crocodile nests in the Tempisque Basin, Costa Rica

“…One may be that the Georges et al (2004) CTE model is lacking in complexity. Neuwald and Valenzuela (2011) document that, if diel temperature variance in painted turtle (Chrysemys picta) nests is large, eggs incubated at female-producing temperatures produce mostly male offspring. Further, Warner and Shine (2011) recover similar findings in jacky dragons (Amphibolurus muricatus), a TSD taxon with two pivotal temperatures that, when experimentally manipulated with 7 4 and 78 degree temperature variance, produced sex ratios that were not predictable by mean incubation temperatures.…”

“…Further, Warner and Shine (2011) recover similar findings in jacky dragons (Amphibolurus muricatus), a TSD taxon with two pivotal temperatures that, when experimentally manipulated with 7 4 and 78 degree temperature variance, produced sex ratios that were not predictable by mean incubation temperatures. Neuwald and Valenzuela (2011) established that within-nest temperature variance of 5°C was required to observe such reversal in turtles. When temperature variance was 3°C, then the expected sex ratios were observed (Neuwald and Valenzuela, 2011).…”