Short heatwaves during fluctuating incubation regimes produce females under temperature-dependent sex determination with implications for sex ratios in nature

Abstract

Patterns of temperature fluctuations in nature affect numerous biological processes, yet, empirical studies often utilize constant temperature treatments. This can limit our understanding of how thermally sensitive species respond to ecologically relevant temperatures. Research on turtles with temperature-dependent sex determination (TSD) provides good examples of this, since nest temperatures from many populations rarely exceed those necessary to produce females under constant laboratory conditions. We hypothesized that exposure to brief periods of warm temperatures (i.e., heat waves) are integral to sex determination in species with TSD, which requires tests that move beyond constant temperatures. We exposed Trachemys scripta embryos from multiple populations and across the nesting season to heat waves of variable durations and quantified sex ratios. We found that embryos from all populations were highly sensitive to brief exposures to female producing temperatures; only 7.9 days of exposure produced a 50:50 sex ratio, but the response varied across the nesting season. From these findings, a model was developed to estimate sex ratios from field temperature traces, and this model outperformed traditional methods. Overall, these results enhance our understanding of TSD and emphasize the importance of using biologically relevant temperatures when studying thermally sensitive processes.

Temperature fluctuations and maternal estrogens as critical factors for understanding temperature‐dependent sex determination in nature

“…In this study, the heat wave treatment (29.5 ± 3°C) was applied during the middle third of development for varying durations (3–30 days), with the remainder of development taking place at a cooler, male producing temperature (27.0 ± 3°C). The results from this work suggest that developing embryos are highly sensitive to heat waves, with an exposure duration of 5 days producing 16% females, and a 50:50 sex ratio produced with only 7.9 days of exposure (Carter et al., ). Although the populations did not vary in their sensitivity to the heat wave, late‐season clutches required approximately 2 days less exposure than early‐season clutches to achieve a 50:50 sex ratio, presumably as a result of having higher yolk estradiol levels (Carter et al., ).…”

“…The results from this work suggest that developing embryos are highly sensitive to heat waves, with an exposure duration of 5 days producing 16% females, and a 50:50 sex ratio produced with only 7.9 days of exposure (Carter et al., ). Although the populations did not vary in their sensitivity to the heat wave, late‐season clutches required approximately 2 days less exposure than early‐season clutches to achieve a 50:50 sex ratio, presumably as a result of having higher yolk estradiol levels (Carter et al., ). The short duration required to produce females is surprising, and confirms that the use of the temperatures experienced during larger swaths of development (e.g., middle third of incubation) are likely to be misleading for sex ratio predictions (Georges, Doody, Beggs, & Young, ).…”

“…A few studies in turtles with TSD have characterized natural patterns of variation in maternal estradiol. For both the red‐eared slider ( Trachemys scripta ) and the painted turtle ( Chrysemys picta ), there is a dramatic increase in the amount of estradiol present within a female's second clutch of the nesting season compared to her first clutch of the nesting season (Bowden et al., ; Bowden, Ewert, Lipar, & Nelson, ; Bowden, Paitz, & Janzen, ; Carter et al., ; Carter, Sadd, Tuberville, Paitz, & Bowden, ; Paitz & Bowden, ). This consistent variation in maternal estradiol levels has been used to investigate the physiological mechanisms underlying the potential effects of maternal estradiol (Paitz & Bowden, ).…”

Agricultural land use creates evolutionary traps for nesting turtles and is exacerbated by mercury pollution

“…Because results were largely consistent between the field and laboratory experiments, our study provides strong causal evidence that the primary proximate mechanism driving agriculturally induced changes in embryonic development and offspring phenotype was lowered average incubation temperatures and daily thermal fluctuations due to shading of nests by crops relative to open canopy conditions. Because the majority of previous studies on development in reptiles have used either constant temperature incubation or perfectly sinusoidal temperature fluctuations, our experimental manipulation of the thermal dynamics within nests in the field, and replication of these dynamic conditions in the laboratory, provides a much needed closer approximation to natural conditions (Bowden et al., , Carter et al., , Warner ).…”

“…Our recent experimental work supported this finding by demonstrating that agricultural crops cool nests, can cause male‐biased sex ratios in snapping turtles, and can interact with maternally transferred mercury to further skew sex ratios (Thompson et al., ). The current study builds on these observations, and on prior knowledge of thermal effects on reptile embryonic development and hatchling phenotype (Bowden, Carter, & Paitz, , Carter, Sadd, Tuberville, & Bowden, , Freedberg et al., , Warner ), in that we (1) document high resolution (hourly) differences in thermal profiles of replicated nests in agricultural (shaded) and nonshaded conditions controlling for genetic and maternal effects, (2) mimic these complex thermal profiles in the laboratory to evaluate the role of temperature in isolation of other variables (such as water availability, maternal effects, and genetics) in determining hatching success and phenotype, and (3) investigate the interactive effects of agriculture and mercury contamination. We predicted that a cooling effect due to crop shading would impact offspring phenotype by prolonging incubation, decreasing hatching body size and posthatch growth rate, and decreasing performance.…”