The future is female: sea turtle sex ratios on a warming planet

In sea turtles, like many species of reptiles, sex is determined by the environmental temperature in which embryos develop. At cooler temperatures, more males are produced, and as temperatures rises, more females are produced. A recent study by Jensen et al., published in January 2018, has proven that in a population of green sea turtles in the Great Barrier Reef, there is a clear female sex bias which is stronger for those originating from nesting beaches in warmer regions. Additionally, by developing historical data, they show that the proportion of females has increased in the past few decades, most probably due to the effects of climate change.
What does this mean for the green turtle populations of the Great Barrier Reef?

A green sea turtle- the focus of a recent study by Jensen et al. Higher temperatures are causing more female offspring to be produced, giving the species a highly skewed sex ratio.
Photo: greatbarrierreefs.com.au

In reptiles, sex is determined by one of two mechanisms: genotypic sex determination (GSD), via sex chromosomes, or temperature-dependant sex determination (TSD), where sex is externally influenced. In TSD, sex is determined by incubation temperature during embryonic development. At the pivotal temperature, males and females are produced in equal numbers. This varies between species and populations, and the transitional range of temperatures that produce completely male or female clutches spans only a few degrees Celsius.

The life history of green sea turtles in the GBR is well known. Green sea turtles mate in shallow waters every two to four years and then lay their eggs on sandy beaches, where they incubate for around 55 days. Clutches usually contain approximately 100 eggs, and females lay several clutches over the nesting season. It is this during this incubation period that the temperature of the beach affects the sex of the offspring produced. In green sea turtles, more females are produced as the temperature increases. It has been suggested that this is an adaptive trait for maximising the reproductive potential of the population- sea turtles tend to nest during the hottest part of the year, leading to a high number of females; this generation will then produce more offspring due to the fact that one male can mate with multiple females.

A map of the Great Barrier reef, showing the nesting and foraging grounds for the two populations of green sea turtles.
Source: Jensen et al. (2018)

Two separate populations of green turtles inhabit the Great Barrier Reef (GBR), but do not share a nesting ground due to their rookeries being located at opposite ends of the reef. There are over 20,000 nesting females in the northern Great Barrier Reef (nGBR)- making it one of the largest sea turtle populations in the world- with most of them nesting on two small coral cays there (Raine Island and Moulter Cay). The southern Great Barrier Reef (sGBR) is also home to nesting females; here the beaches are cooler than in the nGBR.

After incubation, the eggs hatch and hatchlings spend several years in the open ocean before moving to a foraging area. The Holwick Group of Islands in the nGBR is used as a foraging ground for green turtles from both the nGBR and sGBR. Once the turtles reach sexual maturity, they migrate back to their natal beach to breed.

Jensen and his colleagues set out to produce a temporal record of sex ratios at regional rookeries of green sea turtles in the GBR. In July and August of 2014 and 2015, during their period of foraging on the Holwick Group of Islands, a total of 337 green turtles were sampled. Turtles of both sexes and all life stages were hand captured; blood samples were taken for hormonal analysis to determine sex where it was not obvious, and skin samples were taken to locate their natal rookery via genetic analysis. It is possible to establish natal origin of GBR green turtles in this way due to the two populations being so genetically distinct from one another. Turtles were grouped into three age classes: juvenile (4-16 years old), subadult (13-23 years), and adult (>20 years), depending on their size.

So what did Jensen discover?
For the population of green sea turtles at the foraging ground- containing those from both the nGBR and sGBR, as well as some rookeries outside of the GBR- a strong female-biased sex ratio is observed for all age groups. When natal origins of the turtles in the foraging ground were determined, it was clear that the females had originated from across all areas, but juvenile and subadult males groups showed little contribution from the nGBR; adult males showed similar results to those of females.

Relative proportions of male and female green sea turtles at the Holwick Group of Islands foraging ground; strong female-biased sex ratios are observed for all age classes. Natal origins were identified- female turtles across all ages classes originated from both the nGBR (red) and the sGBR (blue), as well as some non-GBR rookeries (black). Orphan haplotypes where natal origin could not be identified are also shown (hatched lines). Source: Jensen et al. (2018)

The data was then split depending on natal origin: in the nGBR, 99.1% of juveniles, 99.8% of subadults, and 86.8% of adult turtles were female (those are ratios of 1M:116F, 1M:554F, and 1M:6.6F, respectively!), whereas in the sGBR, ratios were slightly less skewed, with 67.8% of juneviles, 64.5% of subadults, and 69.2% of adults being female (1M:2.1F; 1M:1.8F; 1M:2.3F). As shown by the extreme ratios in nGBR juvenile and subadult populations, fewer males are being produced in nGBR rookeries than there were previously. Air and sea surface temperature data for the region between 1960 and 2016 back up the fact that sand temperature has increased and eggs have been consistently incubated above the pivotal temperature in this region since 1990.

How much of a problem will the feminisation of green sea turtles in the GBR be in the upcoming years?
Sadly, the results of this study only add to the concern about the overall effects of climate change on the ecosystems of the Great Barrier Reef. The increasing temperatures, especially in the nGBR, will have a massive impact on sea turtle populations- with such long lives, turtles are unlikely to adapt to these changes in time as natural selection requires many generations to take effect. The overall fertility of females in the population will decrease as males become few and far between, not to mention the fact that hatchling survival will decrease due to increased sea levels, habitat warming, and changing weather.

More research needs to be done into the mechanisms of TSD in order to fully understand how green sea turtles will cope with the effects of climate change. For now, though, our priority should be reducing our impact as much as we can and implementing any conservation measures which will help save this species from extinction.

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