Sex runs hot and cold – why does temperature control the gender of Jacky dragons?

By Ed Yong | October 8, 2010 10:00 am

Jacky_dragon

This is an old article, reposted from the original WordPress incarnation of Not Exactly Rocket Science. I’m travelling around at the moment so the next few weeks will have some classic pieces and a few new ones I prepared earlier.

Among Jacky dragons, females are both hot and cool, while males are merely luke-warm. For this small Australian lizard, sex is a question of temperature. If its eggs are incubated at low temperatures (23-26ºC) or high ones (30-33ºC), they all hatch as females; anywhere in the middle, and both sexes are born.

This strategy – known as ‘temperature-dependent sex determination (TSD) – seems unusual to us, with our neat gender-assigning X and Y chromosomes, but it’s a fairly common one for reptiles. Crocodiles are all-male at high temperatures and all-female at low ones, while turtles flip the rules around and produce more males in cooler climes. Assigning gender based on temperature is not uncommon but it is nonetheless puzzling.

Gender seems like an incredibly fundamental physical trait to leave to something as variable as the temperature of your surroundings. How has such a system evolved? What possible benefits could a species receive by switching control of from chromosomes to the environment? Now, a thirty-year old explanation for this puzzling system has finally been confirmed.

The most widely accepted hypothesis was put forward by Eric Charnov and James Bull over thirty years ago. They suggested that TSD occurs when the temperature of the environment affects the success of males and females strongly but differently. Parents can then use local temperatures as a sort of crystal ball, producing more males in conditions that are suited to males, and more females in conditions where they have the edge.

The idea is sound, but testing it has been remarkably difficult. The ideal experiment would involve hatching both males and females at the entire range of incubation temperatures and comparing their success over the course of their lives. Obviously, the very nature of TSD rules out that approach; how do you hatch males at low temperatures if those same conditions, by definition, beget females?

If that weren’t enough, most species that use TSD are large and long-lived. Imagine following a turtle for its entire 60 year lifespan and you begin to see the problem. All that changed this decade when TSD was found in the small and short-lived Jacky dragon (Amphibolorus muricatus). With a lifespan of 3-4 years, here was an animal that could be reasonably studied in experimental conditions.

With one problem down, Daniel Warner and Rick Shine from the University of Sydney solved the other by using hormonal treatments to sunder the link between temperature and sex. Temperature may decide gender but it does so through hormones. The key event is the conversion of testosterone to oestradiol (a relation of oestrogen) by an enzyme called aromatase. This happens at low temperatures and tells developing dragons to become females.

Warner and Shine overrode this process with a chemical that blocks aromatase. With the enzyme disabled, the duo managed to hatch male babies at temperatures that are exclusively female. The hormonally nudged Jackies were physically similar to their male siblings who developed in the normal way; that was essential if they were going to be compared fairly. The duo raised the babies in enclosures that mimicked their natural environments, and waited.

After three consecutive breeding seasons, Warner and Shine found (as predicted) that males sired more offspring on average if they were hatched at an intermediate 27ºC, a normal temperature for them in natural conditions. Males hatched at temperatures that are usually the province of females produced almost three times fewer young. The reverse was true for females; they enjoyed greater reproductive triumphs if they were hatched at a cooler 23ºC or a warmer 33ºC.

Although these results don’t explain why males and females should fare better at different incubation temperatures, they do fully vindicate the Charnov-Bull model. Exactly as predicted, male Jacky dragons produce more young if they hatch at temperatures that usually produce males, and likewise for females.

Such careful fine-tuning has done the lizards well over the course of evolution but it may put them in danger as the globe continues to warm. Like crocodiles, turtles and other reptiles that use TSD, the Jacky dragon may become a casualty of climate change, as rising temperatures lead to an all-female population and no way of producing a new generation.

Reference: Warner, D.A., Shine, R. (2008). The adaptive significance of temperature-dependent sex determination in a reptile. Nature DOI: 10.1038/nature06519

More on sex determination:

Comments (3)

  1. Lyr

    <>

    I wonder if something like this contributed to the extinction of the dinosaurs. (Although the birdlike dinosaurs’ reproductive techniques were probably more, well, birdlike than crocodile-like.)

  2. Hi Ed,

    Not sure why words like “exactly as predicted” and “fully vindicate” give me the jimmies in this context. Words like “exactly” and “fully” or even “vindicated” suggest the success of the experiments was 100% absolute, no-statistical-variation, better-than-chicken-hatchery-standards in line with calculated expectations. In other words Warner and Shine need to have not just knocked the ball out of the park but hit it to the parking lot attendant they pointed to before the swing.

    Otherwise I think words like “as expected” and “supports” might be a better choice.

    Taking you at your word that this reproductive degradation is that predictable (and not, say, an unexpected side-effect of aromatase elsewhere in development) then all kinds of fairly nifty research opportunities arise. For instance you might see an as-yet-unobserved temperature-dependent variation in nest-preparation or egg-laying behaviors by a wide variety of organisms, all designed to optimize male/female ratios. Behaviorists and biochemists could delve into exactly why out-of-temperature-range males fare so poorly compared to their tepid peers. (Is mate selection affected? Sperm production? Fertility synchronization?) Experimentalists could seek hormones similar to aromatase that induced female development at tepid temperatures and then assess whether their reproductive success was also affected. And of course it offers all sorts of juicy guesses about mass extinctions. For instance does the fossil record suggest most surviving dinosaur fossils after the k/t boundary were, say, female, with the result that even those animals that survived the immediate, temperature-changing disaster couldn’t produce enough males to continue the species? (Tough to find enough samples, obviously, but maybe worth it to sift for them.)

    I have to say, though, that I’m a little skeptical that so many species (and by inference their ancestor species) could today be so inflexible on the one hand, while surviving considerable climate variations over the last five million years, let alone the last 50 or 150 million. It certainly looks as though current climate change may happen faster than many species can adapt, but I’m curious how, given more time, the species we see completely (completely!) vindicating Charnov-Bull today would tend to adapt to such a rigid constraint on sex determination.

    But research possibility-wise I have to admit it will be a lot more interesting if my skepticism turns out to be unfounded.

    figleaf

  3. Conover published about this phenomenon in Atlantic silversides with a reasonable explanation for the temperature control: because the fish engage in group spawning, small fish that are male have more reproductive success than females and large fish that are female have more reproductive success than males (cost of gamete production vs. probability of contributing to fertilized eggs). The temperature control allows for fish that hatch earlier have more time to grow before spawning and tend to be females, while the reverse is true for males.

    Conover, D.O. (1984) “Adaptive Significance of Temperature-Dependent Sex Determination in a Fish” The American Naturalist 123(3): pp. 297-313.

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