In most animals the sex of an individual is determined at the moment of fertilization; when the egg and the sperm fuse together it is fixed if that animal will be male or female. Yet in many reptilian groups sex determination is established later during incubation, and the determinant external factor is the incubation temperature of the eggs. In reptiles, this means that the environment plays a crucial role in determining the sex ratio emerging from an egg clutch, and that these animals are very susceptible to alterations in temperature caused, for example, by climate change.
SEXUAL DETERMINATION: GSD VS TSD
In the majority of animal species, sexual differentiation (the development of ovaries or testes) is determined genetically (GSD). In these cases, the sex of an individual is determined by a specific chromosome, gene or allele which will cause the differentiation to one sex or the other. In vertebrates there exists two main types of GSD, the XX/XY system in mammals (in which XX is a female and XY is a male) and the ZW/ZZ system in birds and some fishes (ZW corresponds to a female and ZZ to a male).
Examples of different types of genetic sexual determination systems found in vertebrates and invertebrates, by CFCF.
In the case of reptiles, there is a great variety of sexual determination mechanisms. Some present GSD models; many snakes follow the ZW/ZZ system and some lizards the XX/XY. Still, in many groups the sex of the offspring is determined mainly by the egg incubation temperature (TSD), and therefore the environment plays an important role in the proportion of males and females found in a population.
The eastern bearded dragon (Pogona barbata) is an example of a reptile with GSD, but which is also affected by incubation temperature. Photo by Trent Townsend.
Nevertheless, the genetic and temperature sexual determination are not mutually exclusive. Reptiles with TSD have a genetic base for the ovarian and testicular differentiation which is regulated by temperature. Similarly, it’s been observed that in reptiles with DSG, such as the eastern bearded dragon (Pogona barbata), high temperatures during incubation causes genetically male individuals (ZZ chromosomes) to develop functionally as females. This proves that in reptiles, there is no strict division between GSD and TSD.
TEMPERATURE AND SEX
The incubation period during which the sex of an individual is determined is called thermosensitive period and usually corresponds to the second third of the incubation period, during which temperature must be maintained constant. This critical incubation period usually lasts between 7 and 15 days, depending on the species. After this period the sex of an individual usually cannot be reversed (all or nothing mechanism).
Komodo dragon baby (Varanus komodoensis) hatching. Photo by Frank Peters.
Temperature during the critical incubation period affects the functioning of the aromatase, a hormone which converts androgens (masculinizing hormones) to estrogens (feminizing hormones). At male-producing temperatures, the activity of the aromatase is inhibited, while at female-producing temperatures the activity of the aromatase is maintained.
Graphics of the aromatase’s activity related to gonadal hormones on European pond turtle’s embryos (Emys orbicularis) at 25oC (males) and at 30oC (females), during the critical incubation period, from Pieau et al. 1999.
The TSD is found in all reptile groups except snakes (which have the ZW/ZZ system). In lizards and turtles we can find both genetic-based and temperature-based sexual determination, while in tuataras and crocodilians sex is determined exclusively by temperature. Currently, different patterns of temperature sex determination are known.
This pattern is the simplest one, in which higher incubation temperatures produce one sex and lower incubation temperatures produce the other sex. Intermediate temperatures usually produce individuals of both sexes and very rarely, intersex individuals. This pattern can be further divided in:
- Pattern Ia TSD, in which eggs incubated at warmer temperatures produce high female percentages and eggs incubated at cooler temperatures produce high male percentages. This pattern is found in many species of turtles.
Photo of a European pond turtle (Emys orbicularis), species that follows the pattern Ia TSD; at 25oC or less during incubation only males are born, while at 30oC or more only females are born. Photo by Francesco Canu.
- Pattern Ib TSD, in which the contrary occurs; high temperatures produce males and low temperatures produce females. We find this pattern in some lizards with TSD and in the tuataras.
The tuatara (Sphenodon punctatus) is one of the reptiles that follows the pattern Ib TSD; the pivotal temperature is between 21-22oC, above which males will be born and below which females will be born.
This pattern is a bit more complex than the previous one. In this one, embryos incubated at extreme temperatures (very high or very low) will differentiate to one sex, while the ones incubated at intermediate temperatures will differentiate to the other sex.
Photo of different aged American alligators (Alligator mississippiensis). These reptiles follow the pattern II TSD; at about 34oC males are born, and at higher and lower temperatures, females are born.
This pattern appears in crocodilians, some turtles and in many lizards. Recent phylogenetic studies indicate that this is the ancestral TSD model in reptiles. Some people even argue that all the TSD cases belong to the pattern II, but that in nature temperatures never reach both extremes, although this is yet to be proved.
TEMPERATURE DETERMINED SEX: PROS AND CONS
Even today the evolutionary advantages of the sex determination by temperature are not fully understood. The case of the reptiles is pretty curious because birds, mammals and amphibians determine their sex genetically in most cases, while in reptiles there is a bit of everything.
Currently, there are studies which are being conducted to see if certain temperatures improve the health of males and if other temperatures the health of females. In one of these studies, it was observed that snapping turtles incubated at intermediate temperatures (which produced both males and females) were more active than the ones incubated at temperatures producing only one sex, making them more vulnerable to be attacked by sight-based predators. Currently, there isn’t enough evidence that indicates to what extent these discoveries could be applied. It is possible that reptiles with TSD are able to manipulate the sex of its offspring, altering the proportion of sexual hormones based on the temperature of their nesting site.
Common snapping turtle (Chelydra serpentina) an American fresh-water chelonian, laying its eggs. Photo by Moondigger.
The disadvantages of the TSD are much easier to predict. Any change in the environmental temperature of the nesting areas may affect negatively the populations of a determined species. If a previously shadowy forest is cut down or buildings are constructed in a previously sunny place, the microclimates of the egg clutches of any reptile nesting there will be changed.
Global change, or climate change, represents an additional threat to reptilians with TSD. The rise of the average temperature on the planet and the temperature fluctuation from one year to another, affect the number of males and females that are born in some species of reptiles. This phenomenon has been observed, for example, in painted turtles (Chrysemys picta), in which it has been predicted that a rise of 4oC in their habitat’s temperature could cause the extinction of the species, because only females would be born.
Baby of a painted turtle (Chrysemys picta), species in which incubation temperatures between 23-27oC produce males, and temperatures above and below it produce females (pattern II). Foto de Cava Zachary.
During the elaboration of this entry the following sources have been used:
- Cover photo: Animalspot.
- Halliday & Adler (2007). La gran enciclopedia de los Anfibios y Reptiles. Editorial Libsa.