Temperature Dependent Sex Determination In Turtles Environmental Sciences Essay
Temperature Dependent Sex Determination is a characteristic in reptiles such as turtles. This means that the surrounding temperature determines the sex of the hatchling. Sea turtles nest on beaches, whereas Freshwater turtles nest along river banks. In most cases, a high surface and sand temperature in these areas yields females, and a low temperature yields males. There are various other TSD types as well. In recent years, rising global temperatures and climate change has affected TSD negatively, with sex ratio(s) leaning towards more females. This might have wide ranging effects on viability of a population, including reproductive capability. Adaptations by turtles to deal with this include plasticity in nesting behavior, migration, mating patterns, microevolution and hormonal changes. A long term study encompassing more turtle species and other factors, other than TSD, affecting them is necessary to judge the impact that climate change may have on these organisms.
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There are two types of sex determination in animals. The first is genotypic sex determination (GSD) where the sex is predetermined by sex chromosomes. It is mostly seen in mammals and birds. The second is environmental sex determination-This is where the environment determines the sex of offspring. One type is Temperature Dependent Sex Determination (TSD) which is seen in reptiles [1-2]. This paper will focus on TSD in turtles alone.
In most turtles, high temperatures yield female hatchlings, and low temperatures yield male hatchlings. The temperature of the nest, surface air, and metabolism of hatchlings all contribute to changes in the sex.
In recent years, we have seen an increase in global surface temperatures. Such climate change may affect TSD in turtles, quite dramatically. Physiology, activity, and development of these organisms might be affected by temperature.  Sex is determined by the temperatures experienced during embryonic development and even small temperature changes can produce heavily biased hatchling sex ratios [4-6]. This means that female hatchlings might be produced in larger numbers than males. Understanding climate change and how it might impact species such as turtles is important to conserve them. 
In this paper I will look at effects of climate change on TSD in turtles, with particular focus on the Green Turtle (Chelonia mydas) and the Painted Turtle (Chrysemys picta). I will also examine adaptations in these turtle species, in response to such climate change. This can be in the form of plasticity in nesting, with earlier nesting seasons or nesting under shade areas. This can also be in the form of variations in mating patterns. I will also look at whether such traits are heritable or not.
Turtles exhibit unique nesting behavior. In Sea turtles, females return to the breeding ground where they were born, every year. This is called natal homing . Males lead an offshore life, with their role in reproduction ending with mating. Females may lay two or more clutches of eggs every nesting season. Some may not nest during a particular season too. This nesting season varies from species to species, with some laying eggs in summer and some later on. The only information available about Marine turtles is when they come onshore to nest . Freshwater turtles nest along riverbanks and may nest more number of times as compared to Sea turtles. Once a nest is made and eggs are laid, incubation of eggs occurs from 45-75 days  in Sea Turtles and 72-80 days in Freshwater turtles such as Chrysemys picta . During this time, various incubation temperatures such as metabolic, sand and surface temperature, affect embryogenesis and determine sex of hatchling. This is very important as it may affect turtle numbers, especially in species such as the critically endangered Olive Ridley Turtle.
Temperature dependent sex determination:
In TSD species, the sex of the embryo is determined by the developmental temperature at a particular time of embryogenesis [11-13], which is usually the middle third of development . In turtles there are two main patterns of TSD. In pattern 1, females are produced at high temperatures with males produced at low temperatures.  In pattern 2, females are produced at high and low temperatures with males being produced at intermediate temperatures.  My focus will be on pattern 1 species through this article.
Table 1 show the various turtle species which exhibit the patterns of TSD. Some genera show genotypic sex determination. [2, 15]
Table 1: Sex Determining Mechanism in Various Turtle Species (2, 35)
Turtle Species (Family, genera, or species)
TSD pattern 1
Bataguridae (Pond/wood turtles), Carettochelyidae (Pig-nosed turtle), Cheloniidae(Sea turtles), Dermocheylidae(Leatherback turtle), Emydidae (Pond turtles), Testudinidae (tortoises) [2, 15]
TSD pattern 2
Pelomedusidae(African freshwater turtles), Kinosternidae (Mud/musk turtles), Macroclemys temminckii (Alligator Snapping turtle), Some Bataguridae (Pond/wood turtles) [2, 15]
Platemys(Flat Headed Turtle), Staurotypus(Musk Turtles), Siebenrockiella(Black Marsh Turtle), Kachuga smithii(Brown roofed Turtle), Chelidae(Side Neck Turtles) [2, 15]
Effects of Climate Change:
Climate change is predicted to occur rapidly and raises questions on the impact of such change on nature.  Potential extinction and/or adaptation of various Freshwater and Sea Turtle species to new environmental conditions is of particular interest in this regard.
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Nests face fluctuations in their temperature on a day to day basis.  However, a 4 C rise in temperature for central North America is very likely within the next 100 years . This may vary across different parts of the world, but an increase in temperatures, however small, could have long lasting impacts on Turtle species.
Impacts include skewing of the sex ratio, with more number of females being produced due to an increase in temperature (especially in the TSD pattern 1 species where females hatch at temperatures above 30 C). Hatchling sex ratios are already biased towards females and in all green turtle populations studied to date, these ratios range from 67 to 100 % female . The data available regarding juvenile and adult sex ratios in marine turtles suggest that the female biases seen at hatching are maintained at older life stages [20-22]. Hence, an increase in female hatchlings due to climate change could threaten the viability of turtle populations and also lead to reproductive failure, as fewer males are present.  This might be harmful, especially in smaller populations where the number of males is less than the critical minimum which is required for a fertile population . Larger populations, and those that nest at nesting range extremes where more males are produced, may be less impacted by offspring sex ratio skews , except under the most extreme climate-change scenarios. Another impact would be increased mortality of hatchlings due to these high temperatures. 
In this regard, numerous adaptations might be exhibited by Marine/Freshwater Turtles to such climate change. They include changes in nesting phenology, changes in nest site choice, mating patterns and migration, hormonal changes and microevolution.
Changes in Nesting Phenology-
In a study conducted on painted turtles (Chrysemys picta), it was noticed that Female Turtles of the species tended to lay nests earlier when the previous winter was warm. 
It is not very clear how this happens. However, it might have an effect on when females emerge out of hibernation and might thus effect egg development. [3, 25-27] Egg development is affected by basking of the females and so less sunlight may disrupt it. Less amount of sunlight will also affect the food available for the female's metabolism and in turn affect egg development again. [3, 25-28]
Most females that produced an early clutch, tended to produce a second clutch later on in the season. Earlier clutches tended to have more number of males as the temperatures were cooler. When a second clutch was laid later in the season when temperatures were warmer, more females hatched. This off set the potential impact an earlier clutch would have on sex ratios. This method of adaptation has not been fully explored in all turtle species. 
Studies by Neuwald and Valenzuela in 2011, on Chrysemys picta, suggests that C. picta may respond better to climate change as it is a shallow nesting species, as compared to deeper nesting Sea Turtles [17, 29]. This is because other factors such as shade and nest site choice have a role to play in shallow nests, and not in deeper nests.
Changes in Nest Site choice-
Vegetation cover also had a positive influence on nest sex ratios in studies on Painted Turtles.  Shadier nests produced more male hatchlings than did less vegetated nests.  Females might or might not prefer such vegetation cover. Beaches with lighter sands also produce more males as less heat is absorbed. 
Mating patterns and migration-
Male mating patterns might buffer the impact of climate change. In Green Turtles (Chelonia mydas), it was seen that there were 1.4 reproductive males for every breeding female, despite there being an offspring sex ratio of 95% females.  Males tended to reproduce every year whereas females reproduced every 2-4 years.  Males also migrated between groups of females. This was supported by satellite tracking, and proves that male turtles may visit many females over a lifetime . This shows that relatively equal Operating sex ratios (OSR) were maintained despite a highly skewed female hatchling ratio. The exact reason for such an OSR might be due to this migration or mating patterns.
As climate change increases, migration will also increase, especially in trailing edge populations.  These are marginal communities that might be affected more than populations with large numbers. These trailing edge populations move to better areas as their original nesting sites are disrupted. This model assumes that turtles have newer, better habitats/nesting sites to inhabit. 
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TSD in female and male turtles are independent processes that are controlled by hormones such as estrogen.  Changes in estrogen levels in female turtles will change sex ratios as well.  The potential for this to be an adaptation to climate change is yet to be determined.
The heritability of the above adaptations has been a focus of many studies. Evolution at a small scale or microevolution may stabilize the sex ratio. It might do this by nest site selection or selection of other favorable factors. [3, 33] For example, females might evolve a tendency to nest in shadier or wetter areas and this mitigates the effects of a higher temperature due to climate change.  The evolution of such characteristics might be important now and in the future as well. How fast such evolution can keep up with the ever accelerating climate change is a big question [3, 33-36].
Studies on effects of fluctuating temperatures have been carried out on the painted turtle (Chrysemys picta). Neuwald JL and Valenzuela N in 2011 found that even though under normal conditions a low temperature yields males and high temperature yields females, it is actually more complex when temperatures keep fluctuating. This is especially true under higher temperatures (above 30 C). The mean female producing values were more complex than realized; variations of +/- 5 C from an average of 31 C yielded around 82 % males rather than females.  This was coupled with increased mortality of hatchlings in the clutch at such high temperatures. Fluctuations around lower temperatures such as 26+/- 3 C yielded 100 % males and 26 +/- 5 yielded 8% males. These results might be a more accurate portrayal of climate change, as in reality climate is ever fluctuating .
Turtles might also display other responses to climate change. Some species might change the sensitivity of TSD to temperatures. Some might even alter behavior such as changing reproductive events to suit changes around them.  Some researchers say that TSD in itself is an adaptation to climate change.  The question is why did TSD evolve if it is an adaptation?
In Green turtles adaptations that work include changes in mating patterns, migration and in some cases changes in nesting behavior. Adaptations that might not work include microevolution as Green Turtles are long lived species. Such species cannot regenerate fast enough to keep pace with climatic changes.  In Painted Turtles adaptations that work mostly include changes in nesting phenology such as in the timing of nesting, and area of nesting. Microevolution might work in such shorter lived species as regeneration time is shorter and can keep pace with climatic changes.
Turtles have evolved over 200 million years. Climatic changes have also been a part of this evolution. Long term studies are required to see if Turtles will be able to evolve in tune with the rising temperatures and if so will all species evolve or only some. Studies also need to be done that broadly encompass all species of turtles around the world (not only the two species looked at in this article) and account for factors other than TSD that might be affected by climate.
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