Some like it hot: Temperature-dependent Sex Determination (TSD) in reptiles

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by Ash Wolfe.  Did you know that the surrounding atmospheric temperature of an egg can influence whether a reptile will hatch as a boy or a girl? This is most common in turtles and crocodylids, but also occurs in tuatara and some other lizards. So, rather than genetic sex determination (GSD; like in humans, where you get one X chromosome from your mother and either an X or a Y from your father, XX = female, XY = male), the temperature is responsible for the numbers of males and females. Weird!

This isn’t something that I’m personally working on. Rather, when I was at the Australian Society of Herpetologists conference in January, I listened to a fabulous talk by Dr Lisa Schwanz, and wanted to tell you all about it. Dr Schwanz is a senior lecturer in vertebrate evolutionary ecology at UNSW, and she’s interested in genetics (which is the ‘cool kids’ science nowadays). If you want to find out more about her work, check out this link: http://www.bees.unsw.edu.au/lisa-schwanz.

So we know that TSD affects embryo development, but it’s not the same for every species. For some species, a girl hatches when it’s hot, and in other species females when it’s cold. This diagram shows the 3 different ways that TSD can go (FT = female temp; Tp = point where males and females are equal; MT = male temp):

Sex determination in reptiles
Fig. 1. In Case I (e.g. tuarara), as it gets hotter, more males develop; in Case II (e.g. turtles) the females like it hot; and in Case III (e.g. some lizards), more females develop when it’s hot and when it’s cold, but not when it’s warm. What’s really interesting is that these differences can be just a few degrees, e.g. in turtles, males develop at 22.5-27°C, while females develop at about 30°C.

Considering the fact that NASA declared that 2014 was the Earth’s hottest year since records began1, and the CSIRO and BOM predict that Australia is warming faster than anywhere else in the world2, this could be a problem! Then think about how Australia has over 860 species of reptiles3, 85% of which lay eggs4. While not all of these species use TSD, there’s enough out there for it to be really important.

But do not fret! Dr Schwanz went on in her talk to mention that higher temperatures actually indicate a greater chance of survival for hatchlings. This is mostly because reptiles with TSD also experience differences between males and females and when they mature (and reproduce, thus keeping the cycle going). Have a look at this diagram:

survival and temperature
Fig. 2. Survival vs temperature over five years.

Fig. 2 shows a theoretical model for an animal that can live for 5 (or more) years. Let’s call it the short-lived turtle (using the model in Case II; hotter = more females), in which males live to only 5 years and females live to 10 years. If males only live till 5 years, they need to reproduce early, before they die. Due to their greater fitness from being incubated at a higher temperature when developing in the egg (Fig. 2), females, on the other hand, can wait a little longer before they decide to settle down and have a family. While we always aim for these animals to live a long, long time, in terms of passing on their genes and keeping diversity high (lots of different DNA in a population = good!), an animal only needs to survive to reproduce successfully once. Everything beyond that is a bonus.

This scenario of females out-living males isn’t so bad, because males can mate with more than one female (and normally a clutch of turtle eggs has more than one father). But what happens when females develop more often in cooler temperatures than males? Well, evolution happens… sort of. Long-lived species can shift the activation temperatures for hormones after a few years of very hot or very cold weather (remember, 1 or 2 degrees can make a huge difference) to make sure that they don’t hatch all males or all females. This actually works better for short-lived species (e.g. netted dragons, Ctenophorus spp., which only live for a few years). They have what Dr Schwanz called a buffer, which allows for TSD to shift quite quickly (Fig. 3). The dilemma is that short-lived species will probably be better off than long-lived species because of this buffer, but TSD is more common in long-lived species.

Fig. 3. As it gets hotter or cooler overall, the temperature required to produce males versus females shifts to accommodate this.
Fig. 3. As it gets hotter or cooler overall, the temperature required to produce males versus females shifts to accommodate this.

In summary, TSD is an alternative way for embryos to develop into males and females, and relies completely on the temperature using one of three different ways, depending on the species. It’s more common in long-lived species, but changes in climate are more efficiently managed by short-lived species, and it’s one of the challenges to egg-laying reptiles in the wake of our rising temperatures in Australia.

One thing I’d like to know is how many reptile species in urban areas use TSD? I know that dugites (Pseudonaja affinis) and bobtails (Tiliqua rugosa), the most common large squamates in Perth, use genetic sex determination (GSD), but what about other species? Does TSD affect species living in artificially hot environments such as cities with vast expanses of paved spaces?

These questions are for another time, another person (with better understanding of genetics and environmental sex determination), and another PhD (not mine!).

Special thanks to Dr Lisa Schwanz, who presented this as a plenary talk on the first day of the #ASH15 conference. What a great way to start a show!

References:

1: Cole, Steve, and Leslie McCarthy (2014). “NASA, NOAA find 2014 warmest year in modern record.” Retrieved 9/2/2015 from: http://www.nasa.gov/press/2015/january/nasa-determines-2014-warmest-year-in-modern-record/#.VNh1VvmUd8E

2: CSIRO and BOM (2014). “State of the Climate 2014.” Retrieved 9/2/2015 from: http://www.bom.gov.au/state-of-the-climate/documents/state-of-the-climate-2014_low-res.pdf?ref=button

3: Cogger, Harold G. (2014) “Reptiles and Amphibians of Australia”. CSIRO Publishing, Melbourne.

4: Map of Life (2009). “Viviparity in lizards, snakes and mammals.” Retrieved 9/2/2015 from: http://www.mapoflife.org/topics/topic_331_Viviparity-in-lizards-snakes-and-mammals/

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