Central Bearded Dragon. Credit: Arthur Georges
Central Bearded Dragon. Credit: Arthur Georges

Hot Wild Dragons Set Sex Through Temperature Not Genes

At room temperature, a bearded dragon’s sex depends on two chromosomes. If they have two Z chromosomes, these lizards develop as males. Those with a Z and a W become females. But raise the thermostat up a few notches, and something different happens. If a clutch of dragon eggs are incubated at 34 degrees Celsius, their bodies ignore the usual instructions from their sex chromosomes. Even if half of them are genetically male (ZZ), all of them will hatch as females.

Clare Holleley from the University of Canberra found some of these “sex-reversed” ZZ females in the wild, and bred them with the usual ZZ males. All the offspring from these crosses should have two Z chromosomes, so you might guess that all of them would turn out male.

You’d be wrong. In fact, their chromosomes didn’t matter at all. Instead, their sex depended entirely on the temperature at which they are incubated. Warm clutches produced females; cooler ones produced males. In a single generation, these lizards had evolved a radically different way of determining their sex—one in which their genes completely cede control to the heat of the world.

No one knew that these flips could happen so quickly, but they must surely happen. After all, animals are incredibly varied in their ways of determining sex. In humans, other mammals, and some insects, females usually have two of the same chromosomes (XX), while males tend to have different ones (XY). In birds and some reptiles, including the bearded dragons, the female is the one with different chromosomes (ZW), while the male has identical ones (ZZ). Other reptiles ignore chromosomes altogether and rely on temperature. Turtle eggs are more likely to hatch as males at cooler temperatures, and as females in warmer ones. In crocodiles, this pattern is reversed.

Scientists used to think that these two strategies—genetic sex determination (GSD) or temperature sex determination (TSD)—were mutually exclusive. Animals could use one mode or the other, but never both. That idea was put to rest in 2007, when a team led by Jennifer Marshall Graves experimentally switched bearded dragons from GSD to TSD by raising them at high temperatures. “But we didn’t know if this was something that happens naturally or if the sex-reversed females are fertile,” says Holleley.

Her team solved both mysteries by capturing 131 wild bearded dragons from eastern Australia, and identifying 11 ZZ females among them. They do exist in the wild, they can mate with males, and they can themselves be mothers of dragons. When Holleley incubated their eggs at 30C or under, they all hatched as males. At 36C, they were all female. At intermediate temperatures, she got a mix. In just one lab-bred generation, the W chromosome had completely disappeared, and the dragons had switched completely to TSD.

“It is often thought that once a species veers down the path of chromosomal sex determination, there’s no going back,” explains Melissa Wilson-Sayres from Arizona State University. That’s because the two chromosomes develop sex-specific versions of important genes, and one of them—such as the Y in humans—loses so many genes that it becomes small and stunted. This supposedly creates an inescapable rut. “But this paper suggests that not only is it possible for a population jump out of the chromosomal sex determination rut, but that it actually occurs in the wild,” says Wilson-Sayres. “It’s  fantastic because it shows how much variation can exist right below our noses.”

“This makes me think of the statements I’ve seen about trans individuals not being “truly male” or “truly female”, because of their (presumed) set of sex chromosomes,” she adds. “This research tells us that even with chromosomal sex determination, exceptions occur all the time. In the bearded dragon, the exception may even be a benefit, as ZZ females lay more eggs that ZW females. This tells us that we’re thinking much too simply if we say with confidence that only XX is female and XY is male.”

Holleley doesn’t understand exactly how the lizards flip from GSD to TSD because the genetics of sex determination are still a mystery in reptiles. In mammals, the Y chromosome has a gene called SRY that acts as a master sex-determining gene—if individuals have it, they’re usually male, and if not, they’re usually female. In birds, the equivalent gene is called DMRT1. But the reptilian counterpart is still a mystery. “We’ll have to figure out what the gene is, and how it’s regulated by temperature,” says Holleley.

The consequences of her discovery are also unclear. In the wild, the switch from GSD to TSD would be more gradual than what Holleley saw in the lab. Still, “there are many reasons why we think that if you get an extreme climatic event, and sex reversal starts happening, it’ll snowball,” she says.

First, as Wilson-Sayres noted, the sex-reversed ZZ females produce twice as many eggs as the usual ZW ones. Second, the offspring of the ZZ females are more likely to reverse sexes themselves—that is, males will hatch as females at lower temperatures than their mothers did. The third reason is more complicated. In a warmer world, ZW individuals all still become females but so do some ZZ individuals. This means that males become rarer. It also means that mothers become more successful if they have more sons, since those sons face less competition and can find mates more easily. So evolution should push mothers to have more ZZ male offspring.

These three effects all spell trouble for the W chromosome and—provided the climate stays very hot—should eventually eradicate it. In the end, all the dragons should be ZZ and all of them should rely on TSD.

What happens next? It all depends on the threshold temperature at which all-male broods give way to all-female ones. If the threshold is a sensible one, and keeps in step with environmental changes, then the dragons will be fine. They’ll just stick with TSD as many other reptiles do. But if the threshold is too low, and the world keeps getting hotter, then trouble looms. “They could potentially get more and more female-biased, and if you end up with all females, you’ll go extinct,” says Holleley.

Reptiles have obviously lived through many extreme fluctuations in climate, and they’re still around. Indeed, Holleley’s discovery does suggest that “reptiles may have greater capacity to cope and compensate for climate change than previously appreciated.” Then again, the current rate of warming is far steeper than what they would have encountered in the past. It’s a brave new world; how reptiles will fare in it is anyone’s guess.

Reference: Holleley, O’Meally, Sarre, Graves, Ezaz, Matsubara, Azad, Zhang & Georges. 2015. Sex reversal triggers the rapid transition from genetic to temperature-dependent sex. Nature http://dx.doi.org:10.1038/nature14574