Sex determination

Some like it hot (and some don't)

There is a widely accepted theoretical explanation for why sex in some species is determined at the embryo stage by environmental factors such as temperature. That theory is now supported by experiment.

How the sex of offspring is determined seems simple enough if you don't look beyond ourselves. For humans, the system is genotypic: two X chromosomes, and you're female; an X and a Y, and you're male. There are plenty of variants of this system, but in many reptiles an entirely different mechanism applies: sex is determined by the temperature of the incubating egg, and clutches can be all-male, all-female or somewhere in between.

On page 566 of this issue1, Warner and Shine answer a long-standing question about the evolutionary significance of sex-determining mechanisms in reptiles. Four decades ago, it was reported2 that incubation temperature determined sex in the African red-headed rock lizard, an observation that seemed to fly in the face of evidence for sex chromosomes in several other reptiles3. Scientists soon realized that both types of sex-determining system were not only widespread in reptiles but also highly developed, and at the time they seemed to be mutually exclusive4. What has remained a puzzle is whether there is an adaptive benefit of temperature-dependent sex determination (TSD) and how that benefit might work. Using an Australian lizard, Warner and Shine find the long-sought evidence of an adaptive benefit of TSD.

The main model suggested to explain the advantage of TSD, or of any sex determination in response to an environmental cue, takes an idea from Trivers and Willard5. This posits that in some circumstances a species will have greater reproductive fitness if the offspring are male instead of female, whereas in other circumstances the reverse is true. For example, if there is a premium on large size for male reproduction, an offspring deprived of food such that it will be born small and remain smaller than average throughout its life may have higher fitness as a female than as a male. From there, the argument for why sex should be environmentally determined is merely that, if there is a strong benefit to controlling offspring sex ratio to suit the circumstances, natural selection will favour a mechanism to do so6.

In reptiles, sex is determined during the embryonic stage. For environmental sex determination to fit this model, something happening to the egg or embryo must carry over into adult fitness, and the effect must be one that works differently for males than females, so mere survival to hatching does not provide an explanation. The puzzle is that, because so much growth happens between hatching and maturity in a reptile, it would seem that all effects of embryonic temperature would be erased by adulthood.

There has been no shortage of ideas for how this model6 could apply to reptiles, from supposing any of several direct effects of incubation temperature on egg-to-adult fitness, to allowing mothers to manipulate offspring sex ratio by choice of nest site7. However, until now all explanations have relied on inferences about fitness effects, not measurements.

By integrating several techniques for lab and field studies, and with a careful choice of study organism, Warner and Shine1 show that incubation temperature affects lifetime fitness and does so differently for males and females. Their study organism was a short-lived lizard, the jacky dragon (Fig. 1). The use of a short-lived species is important because the differential effects of incubation temperature are expected to be strong in short-lived species, and not necessarily so in long-lived ones.

Figure 1: The jacky dragon, Amphibolurus muricatus.
figure1

D. GARNETT

This is a species of reptile in which the sex of the offspring is determined by the egg-incubation temperature, and was the experimental model chosen by Warner and Shine1. The jacky dragon's comparatively short lifespan of some 3–4 years makes it especially suitable for sex-determination research.

The next trick required a way of producing both sexes across a wide range of incubation temperatures. The theory holds that only the sex of relatively higher fitness should be produced at any one temperature, and indeed, TSD is often so extreme that only one sex is produced across a wide range of incubation temperatures. Thus a test of the theory requires producing both sexes at temperatures where one sex is normally absent. Male jacky dragons are produced in only a narrow, intermediate temperature range. So to produce males at high and low temperatures, Warner and Shine used the now-common method of applying chemicals to the egg that interfere with steroid hormone biosynthesis, in this instance the aromatase inhibitor fadrozole8.

Eggs were incubated in the lab at one of three temperatures (low, intermediate, warm), and the hatchlings were released into outdoor enclosures (about 30 lizards in each of 6 enclosures). The lizards were allowed to grow up, mate and produce offspring in these enclosures over a period of 3.5 years. To measure fitness — reproductive success — Warner and Shine established parentage of each of the offspring by genotyping DNA microsatellites. All offspring born in the enclosures were unambiguously assigned to specific parents, thus bypassing any indirect measures of presumed mating success and fecundity.

Lifetime reproductive success showed some surprises. For females, it was expected, first, that warmer incubation temperatures would lead to larger body size (because warmer temperatures lead to earlier hatching); and, second, that body size would correlate strongly with fecundity. Thus female fecundity should increase with incubation temperature. This compound expectation was only partly supported: female lifetime fitness was highest at the warmest temperature, but no appreciable fitness difference was found between the intermediate and low temperatures. For males, there was no obvious basis for prediction, but males from intermediate temperatures had appreciably higher fitness than males from low and warm extremes. In all, the fitness measures matched the theory, but most of the fitness effects of temperature defied intuition.

The study1 provides directions for future work. The most important concerns the mechanistic bases by which incubation temperature affects male versus female fitness. There is accumulating evidence that incubation temperature in TSD lizards has a variety of behavioural, anatomical and physiological effects, including directly acting on brain development9,10. In addition, even though offspring are either male or female in terms of their gonads, hormone levels throughout life vary according to the individual's incubation temperature, further contributing to a gradation of attributes that translate into fitness differences within a sex caused by incubation temperature. To the extent that such interactions exist, TSD may have evolved to be somewhat self-reinforcing, in essence providing the basis for much of its own benefit. It will thus be interesting to solve the mechanistic link between temperature and fitness, to augment the observations that Warner and Shine have at last provided to resolve the riddle of reptilian sex determination.

There is also a wider picture to this line of research. It has been suggested that sex determination by temperature or other environmental factors is ancestral to genotypic sex determination, and that elements of TSD can be found in mammals11. Even in humans, conditions during gestation have lasting effects throughout life, with recent work indicating a connection with coronary disease, obesity, diabetes, cancer, cognitive dysfunction and infertility12.

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Crews, D., Bull, J. Some like it hot (and some don't). Nature 451, 527–528 (2008). https://doi.org/10.1038/451527a

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