At 27.9 °C, roughly equal numbers of female and male turtles will emerge from the nests of the Chinese pond turtle Mauremys reevesii. Slightly warmer, and more females will hatch; a little cooler, and there will be more males.
Developing reptile embryos that have temperature-dependent sex determination were long thought to passively accept their weather-based fate. But now, new research suggests that at least in M. reevesii, embryos can move around to find slightly cooler or warmer regions within their eggs, and thereby have some control over the sex they develop into. The authors propose that this ability may help offset drastic, population-wide shifts in sex ratios that are occurring due to climate change. The findings appear today (August 1) in Current Biology.
“I find it fascinating that [embryonic movements] may be an important contributor to the production of equal numbers of males and females at intermediate conditions in the wild,” writes evolutionary biologist Nicole Valenzuela of Iowa State University to The Scientist in an email. “It is quite a novel finding.”
Behavioral ecologist Wei-Guo Du of the Institute of Zoology at the Chinese Academy of Sciences in Beijing and his colleagues found in 2011 that turtle embryos can move towards warmer regions of their eggs, and suspected that this could influence offspring sex. However, other researchers have since challenged this idea, arguing that there isn’t a strong enough thermal gradient across reptile eggs and that the embryos simply don’t have the ability to move.
To test their hypothesis, Du and his colleagues started by measuring how much temperatures can vary between the two ends of an egg. In eggs they dug up from a dozen turtle nests by an outdoor pool at a commercial turtle farm they found “dramatic” differences in temperature, Du says: the difference was 1.2 °C on average and could be as high as 4.7 °C.
To find out if developing turtle embryos cold move towards warmer or cooler regions within the egg, the scientists disrupted their ability to sense temperature by applying to the outside of the egg a chemical called capsazepine, which reportedly blocks ion channels that act as heat sensors in crocodiles and lizards.
In the lab, the team placed a heat source at one end of the capsazepine-treated eggs, held a light to the eggs so they could view their contents, and marked the embryos’ position within the egg. After one week, they observed that these embryos had barely budged, whereas untreated embryos had moved by a few millimeters towards the warmer end of the egg.
To see if this would have any effect on the sex ratio of clutches, the team removed eggs from around 20 nests, each with eight eggs on average. They treated half of them with capsazepine, and placed all of them back into nests at random. Three months after hatching, they sexed the animals by inspecting their gonads.
The effect of capsazepine relative to untreated eggs varied by season. When the eggs developed in colder months, the majority of both treated and untreated eggs hatched as males, and in hot months nearly all of them were female.
But when ambient temperatures hovered around 28 °C—the “pivotal” temperature at which males turn female—the difference between untreated and treated eggs became apparent: capsazepine-treated eggs skewed heavily male when the temperatures dipped a little below that temperature, and female at slightly warmer temperatures. Untreated eggs, on the other hand, appeared to resist this shift, producing a 1:1 sex ratio.
The authors propose that untreated embryos—which have the ability to sense temperature—are offsetting heat variations by moving towards the cooler end of the egg at warmer temperatures, and vice versa. This expands the range of temperatures at which both sexes can exist in relatively even ratios. “Natural selection favors behaviors that increase an individual’s viability—in this case, by enabling it to develop as the sex that will benefit most from the current conditions,” Du writes in an email.
But this only works when ambient temperatures are close to “pivotal” temperatures, and as long as temperatures vary across the egg. It’s “one potential mechanism” that complements other strategies turtles have in place to handle climatic variations, such as mothers’ choice of shadier or deeper nests, Du explains.
Fredric Janzen, an evolutionary biologist at Iowa State University, is yet to be convinced that embryos can shift around the egg and influence their sex. As he and others have argued previously, the idea is implausible for several reasons. “In a real nest, they’ve only moved basically a millimeter—a millimeter in a thirty-four-millimeter egg . . . there’s no thermal gradient in a millimeter,” he explains. “And really, there’s no way for them to move because the yolk sac is large, it’s surrounded by an impenetrable membrane—so it’s not like these things can just swim. They’re stuck between an airspace and a big yolk,” adds Janzen, who has collaborated with one of the paper’s coauthors but wasn’t involved in the current study.
It may be plausible that embryos are passively pulled towards warmer temperatures, like any object in a fluid, Janzen says. But he can’t think of any explanation why they would be disproportionately drawn to cooler temperatures under warmer conditions.
Both Janzen and Valenzuela agree that the results would be more convincing had the authors tracked the embryo movement more closely, rather than merely recording the embryos’ positions before and after a week-long period—particularly as nest temperatures in the wild can fluctuate greatly throughout a given day. “It is unclear if embryos moved within the week between measurements,” notes Valenzuela, who has also collaborated with one of the study’s coauthors in the past but wasn’t involved in the new research.
In the paper, Du and his colleagues stress the potential for embryo thermoregulation to help ameliorate the effects of climate change. Using a climate change model to predict the sex ratio of Chinese pond turtles, they find that the ability to thermoregulate leads to more even sex ratios than when thermoregulation is not taken into account. But Valenzuela notes that reptile embryos’ capacity to do so is likely extremely limited, given that their influence on their sex is restricted to a very narrow range of temperatures.
Extraordinary results warrant skepticism, Janzen concludes. “I really look forward to the possibility that these findings might be replicated by scientists studying other species with this temperature-dependent sex determination. That would certainly give a better feel for the generality of their results.”
Y. Ye et al., “The embryos of turtles can influence their own sexual destinies,” Current Biology, doi:10.1016/j.cub.2019.06.038, 2019.
Katarina Zimmer is a New York–based freelance journalist. Find her on Twitter @katarinazimmer.