Temperature-Dependent Sex Determination in Reptiles and Fish

Temperature-Dependent Sex Determination in Reptiles and Fish

In most vertebrates, the sex of an offspring is decided by chromosomes at the moment of fertilization. However, some species utilize a fascinating biological mechanism known as temperature-dependent sex determination (TSD). This form of environmental sex determination (ESD) occurs when the ambient temperature experienced during embryonic or larval development dictates whether an individual becomes male or female.

While most commonly associated with reptiles and teleost fish, TSD has also been reported in certain species of shrimp. Unlike genetic sex determination (GSD), where sex is fixed by DNA, TSD allows the environment to play a primary role in shaping the population's sex ratio.

Patterns of temperature-dependent sex determination (TSD) in reptiles. Pattern I in this image actually depicts Pattern IA - which is found in turtles, e.g. Red-eared slider turtles (Trachemys scripta), Olive Ridley sea turtles (Lepidochelys olivacea), or Painted turtles (Chrysemys picta). Pattern II has been found in American alligators (Alligator mississippiensis and Leopard geckos (Eublepharis macularius).[13]
Patterns of temperature-dependent sex determination (TSD) in reptiles. Pattern I in this image actually depicts Pattern IA - which is found in turtles, e.g. Red-eared slider turtles (Trachemys scripta), Olive Ridley sea turtles (Lepidochelys olivacea), or Painted turtles (Chrysemys picta). Pattern II has been found in American alligators (Alligator mississippiensis and Leopard geckos (Eublepharis macularius).[13]

Key Facts

  • Definition: TSD is a process where incubation temperatures during development determine the sex of the offspring.
  • Occurrence: Primarily found in reptiles (turtles, crocodilians, some lizards) and teleost fish.
  • Thermosensitive Period: The critical window, typically the middle third of embryonic development, when temperature affects sex.
  • Mechanisms: Potential drivers include epigenetic regulatory pathways and cortisol-mediated pathways.
  • Adaptive Value: TSD may maximize offspring fitness by matching sex to the most favorable environmental conditions.

The Mechanics of TSD

The Thermosensitive Period (TSP)

Not all stages of development are susceptible to temperature changes. The thermosensitive period is the specific window—usually the middle third of embryonic development—during which the temperature of the environment triggers the commitment to a specific sex. Histological studies on turtles have helped researchers pinpoint the exact chronology of when gonads differentiate during this phase.

Biological Pathways and Epigenetics

Although the exact molecular mechanisms are still being researched, scientists believe that epigenetic regulatory pathways and cortisol-mediated pathways are central to TSD. For example, in red-eared slider turtles, an epigenetic modifier called KDM6B (a histone H3 lysine 27 demethylase) activates male development by binding to the promoter of the DMRT1 gene. Research has shown that knocking down KDM6B at 26 °C can trigger a male-to-female sex reversal in most surviving embryos.

Some reptiles use incubation temperatures to determine sex. In some species, this follows the pattern that eggs in extremely high or low temperatures become female and eggs in medium temperatures become male.[14]
Some reptiles use incubation temperatures to determine sex. In some species, this follows the pattern that eggs in extremely high or low temperatures become female and eggs in medium temperatures become male.[14]

Examples Across Species

Reptiles

  • Turtles: Species like the Red-eared slider, Olive Ridley sea turtle, and Painted turtle often exhibit patterns where specific temperature ranges produce one sex over the other.
  • Crocodilians: American alligators use TSD, where gonadal fate is influenced by the levels of testicular genes and estrogen signaling. Critical commitment for testicular development occurs during stages 24-26.
  • Lizards: In Australia's bearded dragon lizards, high temperatures can override genetic signals. Some ZZ-chromosomal individuals (typically male) have developed as females capable of bearing offspring due to heat.

Fish and Other Species

Teleost fish frequently exhibit TSD, and some reports suggest similar mechanisms in shrimp. In these species, extreme temperatures can shift sex ratios, though researchers caution that these effects must be distinguished from those experienced in natural wild environments to be evolutionarily relevant.

Adaptive Significance and Evolution

The Charnov-Bull Hypothesis

The Charnov-Bull model suggests that TSD is an evolutionary advantage because it allows the sex that benefits most from a particular incubation temperature to be produced. This has been supported by studies on Jacky Dragon lizards, where hatching temperatures that naturally produce a specific sex were found to maximize the fitness of that sex.

Similarly, research on Painted turtles showed that hatchlings from single-sex producing temperatures had higher first-year survivorship and better energy efficiency than those from mixed-sex nests.

Transition from ESD to GSD

Environmental conditions can drive the evolution of sex-determination systems. In spotted skinks, lowland populations (with constant temperatures) utilize TSD. However, highland populations—where temperatures fluctuate wildly and the activity season is shorter—have evolved GSD. This prevents skewed sex ratios that would otherwise occur in unstable climates.

Feature Genetic Sex Determination (GSD) Temperature-Dependent Sex Determination (TSD)
Primary Driver Chromosomes/DNA Ambient Temperature
Timing of Determination Fertilization Thermosensitive Period (Development)
Flexibility Fixed Plastic/Environmental
Common Examples Mammals, Birds, Highland Skinks Turtles, Alligators, Lowland Skinks

Frequently Asked Questions

What is the thermosensitive period?

The thermosensitive period is the critical window during the middle third of embryonic development when the temperature of the environment determines the sex of the offspring.

Can an animal's sex change due to temperature?

Yes, in some species. For example, high temperatures in bearded dragon lizards can cause individuals with male (ZZ) chromosomes to develop as females.

How does TSD differ from chromosomal sex determination?

Chromosomal determination is fixed at fertilization by the genetic material provided by the parents, whereas TSD is an environmental process that occurs during the incubation of the egg.

Why would a species evolve to use temperature instead of genes for sex?

According to the Charnov-Bull hypothesis, TSD allows a species to produce the sex that will have the highest fitness or survival rate based on the specific environmental conditions of the nest.

Which animals are most known for having TSD?

TSD is most prominently observed in reptiles, such as turtles and crocodilians, as well as in various species of teleost fish.

References

  1. Ido Pen; Tobias Uller; Barbara Feldmeyer; Anna Harts; Geoffrey M. While & Erik Wapstra (2010). "Climate-driven population divergence in sex-determining systems". Nature. 468 (7322): 436–439. Bibcode:2010Natur.468..436P. doi:10.1038/nature09512. hdl:11370/a89e2047-41c9-4c84-bd5e-9637fe57aa52. PMID 20981009. S2CID 4371467.
  2. Warner DA, Shine R (2008). "The adaptive significance of temperature-dependent sex determination in a reptile". Nature. 451 (7178): 566–568. Bibcode:2008Natur.451..566W. doi:10.1038/nature06519. PMID 18204437. S2CID 967516.
  3. Bachtrog, Doris; Mank, Judith E.; Peichel, Catherine L.; Kirkpatrick, Mark; Otto, Sarah P.; Ashman, Tia-Lynn; Hahn, Matthew W.; Kitano, Jun; Mayrose, Itay (2014-07-01). "Sex determination: why so many ways of doing it?". PLOS Biology. 12 (7) e1001899. doi:10.1371/journal.pbio.1001899. ISSN 1545-7885. PMC 4077654. PMID 24983465.
  4. Tree of Sex Consortium (2014-01-01). "Tree of Sex: a database of sexual systems". Scientific Data. 1: 140015. doi:10.1038/sdata.2014.15. PMC 4322564. PMID 25977773.
  5. Ospina-Alvarez, Natalia; Piferrer, Francesc (2008-07-30). "Temperature-dependent sex determination in fish revisited: prevalence, a single sex ratio response pattern, and possible effects of climate change". PLOS ONE. 3 (7) e2837. Bibcode:2008PLoSO...3.2837O. doi:10.1371/journal.pone.0002837. ISSN 1932-6203. PMC 2481392. PMID 18665231.