25. Jan, 2018

Teenager female turtles dominate the northern Great Barrier reefs

Green sea turtles (Chelonia mydas) migrate long distances between feeding and nesting sites; and some swim more than 2,600 kilometers  to reach their spawning grounds. Female turtles can store sperm from a single mating for the entire nesting season and males visit the breeding areas every year, attempting to mate.  The eggs are round and white, and about 4-5 cm in diameter and hatch  in the sand. The hatchlings remain buried until they all emerge together at night after around two months.Then they rush instinctively over the beach to the waterline. Nests may contain up to 200 eggs. But only few turtles reach adulthood in the  oceans where they are a favorite prey  for  various predators. The highest rate of predation occurs in the water within the first 30–60 min of swimming as they pass through the cordon of predators found in the shallow water surrounding natal beaches

Left: Top: two separate nesting sites  of green sea turtles along the Great Barrier Reef. ( adapted from **). 

Along the east coast of Australia female and male green turtles mate in the vicinity of their nesting beach.  The Northern Great Barrier Reef (GBR) is home to one of the largest green turtle populations in the world, with an estimated female population size of around 200,000 nesting females. Furthermore, two genetically distinct breeding populations of green turtles are found at the opposite ends of the Great Barrier Reef: the southern Great Barrier Reef (sGBR) stock and the northern Great Barrier Reef (nGBR) stock, with virtually no nesting occurring along the middle part of the GBR (see picture left). On the average 80% of the turtles at the GBR are female and 20% male.

Sex determination  in turtles  Reptiles are related to birds and  have  roamed the earth for more than 300 million years. Most reptiles including sea turtles do not have sex chromosomes. Instead, sex of newborns depends on temperature-dependent sex determination  (TSD). TSD relates to temperatures experienced during the middle third of embryonic development. It was already known to hold for the green as well as the painted turtle (Chrysemys pica)  populations in areas where cooler summers always  produced mostly male, and warmer summers mostly female  turtle offspring (see Janzen *). Janzen also found that nests of the common snapping turtle (Chelydra serpentina)  incubated at 26°C produced 100% males, at 30°C produced 100% females, and at 28°C produced equal numbers of females and males.

How does TSD work? Pivotal temperatures are species-specific temperature ranges in which males and females are produced in equal number. The pivotal temperature is heritable but only a few degrees Celsius  are needed to drastically alter this ratio to  produce 100% males or 100% females spans. It still remains unclear how the developing embryo detects a thermal stimulus that apparently directs its sexual fate. Microscopic studies of the embryo gonads have established  that steroid hormones could start the process once the temperature change is detected.  In some turtles the critical temperature-dependent component appears to be synthesis of the enzyme aromatase, which converts androgens, such as testosterone, into estrogens. At higher temperatures, increased aromatase activity produces more estrogens, which biases the sex ratio toward more females. 

TSD and fitness A common pattern of TSD in turtles is that warmer temperatures favor development of female and colder temperatures development of male  hatchlings. This pattern would make sense from the point of view of  natural selection if females  gain more in lifetime fitness by developing in higher water temperatures compared to male turtles. Which would create a stronger tendency of females than males to avoid cooler beaches. For example, warmer temperatures may lead to a stronger greater adult body size, which has a greater effect on female fecundity than on male fertility. In line with this theory Janzen reported that hatchlings from the all-male and all-female producing temperatures had significantly higher first-year survivorship than did consexuals from the incubation temperature that produced both sexes from the incubation temperature that produced both sexes.

Climate warming and GBR nesting Species with TSD have existed for millions of years and coped with the selective pressures of a changing environment through adaptive changes of heritable traits. However, it is unlikely that these traits would evolve rapidly enough to keep pace with the current rate of climatic warming.  A recent Australian/American  study carried out on 441 green turtles of the GBR (**) has shed more light on the possible impact of climate change on changing sex ratio’s of the green turtles colonies of  the GBR. Blood and tissue samples were collected from the turtles to determine sex, steroid hormones and DNA. The study found a strong sex bias depending on the location of the GBR where eggs hatched. In the cooler southern GBR nesting beaches there was a moderate female sex bias (65%–69% female) in turtles, but  turtles that originated from  northern GBR nesting beaches were extremely female-biased (99.1% of juvenile, 99.8% of sub-adults, and 86.8% of adult-sized turtles; see also figure above, lower panel). The study further indicated that northern GBR green turtle locations  have  been producing primarily females for more than two decades and that the proportion of females has increased in recent decades.

Conclusion With average global temperature predicted to increase 2.6C by 2100, many sea turtle populations are in danger of high egg mortality and female-only off-springs. A high female bias  as such might not create a problem, since only few males are needed to fertilize an entire colony of females. But an extreme female bias would create a problem in finding a male at all, and/or  lead to genetic impoverishment due to lack of genetic variation in a relatively small group of males. Visits of breeding males from other populations  might mitigate extreme feminization, but this would  be less likely  to occur at the northern GBR,  where visits of male turtles from the south are less likely to occur.

Extreme incubation temperatures not only produce female-only hatchlings but also cause high mortality of developing clutches. A some beaches in  Florida the strain of surviving at elevated temperatures and resulting heat stress seems to  weaken the hatchlings and  slow down their  run to reach the shoreline in time. Researchers are  now exploring plans to cool the nests, like using shade cloth or putting water on top of them.

Sources

*Janzen, F.J. (1994). Climate change and temperature-dependent sex determination in reptiles. Proc. Natl. Acad. Sci. USA 91, 7487–7490.

Janzen,F.J. (1995) Experimental evidence for the evolutionary significance of temperature-dependent sex determination, Evolution 49 864 – 873.

**Jensen, M.P. et al. (2018), Environmental Warming and Feminization of One of the Largest Sea Turtle Populations in the World.  Current Biology 28, 154–159

***Spencer, R. J.; Janzen, F. J. (2014). "A novel hypothesis for the adaptive maintenance of environmental sex determination in a turtle"Proceedings of the Royal Society B281

 Hake, L. & O'Connor, C. (2008) Genetic mechanisms of sex determination. Nature Education 1(1):25

Warner DA, Shine R (2008). "The adaptive significance of temperature-dependent sex determination in a reptile"Nature. 451(7178): 566–568. . 

 Pen, Ido,  et al.  (2010). "Climate-driven population divergence in sex-determining systems". Nature. 468: 436–439. 

Valenzuela, Nicole; Fredric J. Janzen (2001). "Nest-site philopatry and the evolution of temperature-dependent sex determination" (PDF). Evolutionary Ecology Research. 3: 779–794. Retrieved 7 December 2011

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