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Change is good...just ask a baby turtle

 Change is good, or so the old adage goes. But is that really true, or is it something said to create a silver lining when the world seems to be shifting at an uncomfortable pace. Not all change is good (just ask the climate), but for some creatures, a little variance can go a long way. Take, for example, the common snapping turtle (Chelydra serpentina). A recent study by Leivesley and Rollinson (2021) found that mimicking natural temperature fluctuations in incubating eggs had a beneficial effect in early-age immune response. The authors were interested in using immune response as a marker of fitness under the Charnov-Bull model. Their experimental design included four groups: a male promoting temperature (MPT; 24⁰ C) and a female promoting temperature (FPT; 28⁰ C), each split into constant and fluctuating temperature regimes. Half of the eggs in each group were treated with an aromatase inhibitor, which effectively prevents female development even at the FPT. The idea is that if immune response is a good indicator of fitness under the Charnov-Bull model, then males raised at MPT and females raised at FPT should have higher immune response compared to aromatase inhibited males at FPT. Although the authors did not find evidence for this, their secondary finding that fluctuating temperatures boost immune response grants support to a growing body of evidence that traditionally used constant incubation temperatures fail to capture important developmental effects.

This issue was introduced to us in class earlier this semester, with the implication that it could drastically change what we already know about temperature-dependent sex determination (TSD). So far, most experimental studies on TSD incubate eggs at constant temperatures, but this is far from how the environment operates. The role of fluctuating nest temperatures could have important yet unforeseen impacts on embryo development. And to prove my point, we must turn to another chelonian companion, the diamondback terrapin (Malaclemys terrapin). Fluctuating nest temperature has a two-fold impact on this species: reduced developmental rates and larger hatchlings. In fact, fluctuating temperatures more closely modeled cooler, constant incubation temperature, which similarly slowed developmental rate. Higher constant temperatures sped up development and produced smaller hatchlings (Rowe et al. 2020). The daily dips in temperature under a fluctuating regime thus seem to help maintain slower development important for producing big hatchlings. In an unforgiving and oftentimes cruel natural world, size does matter, and evidently so does fluctuation.

It is not just turtles that yield these benefits. Lizards also seem to benefit, as was found in brown anoles (Anolis sagrei), where fluctuating nest temperatures enhanced hatchling performance and survival with minimal developmental effects (Hall and Warner 2020). Clearly, the importance of natural variation is more widespread than once thought, which should become clearer as more and more evidence supporting the importance of nest temperature fluctuation comes to light. And while some change is good, it is important to keep in mind that too much change can be catastrophic. The world is rapidly shifting towards a warmer and more stochastic climate, and many species may not be able to handle these changes. A shift of 3⁰ C (from 31⁰ C to 34⁰ C) results in a mortality increase from 0% to 33% in diamondback terrapin eggs; another 3⁰ C increase results in total mortality (Rowe et al. 2020). In order to effectively protect temperature sensitive species, it is important to understand how they are impacted by temperature variation and discover when change shifts from something beneficial to being too much of a good thing.

 

Citations

Hall, J.M. and D.A. Warner. 2020. Ecologically relevant thermal fluctuations enhance offspring fitness: biological and methodological implications for studies of thermal developmental plasticity. Journal of Experimental Biology 223(19): jeb231902.

Leivesley, J.A. and N. Rollinson. 2021. Maternal provisioning and fluctuating thermal regimes enhance immune response in a reptile with temperature-dependent sex determination. Journal of Experimental Biology 224(5): jeb237016.

Rowe, C.L., D. Liang, and R.J. Woodland. 2020. Effects of constant and fluctuating incubation temperatures on hatching success and hatchling traits in the diamondback terrapin (Malaclemys terrapin) in the context of the warming climate. Journal of Thermal Biology 88: 102528.

Comments

  1. Very interesting! I think a lot about this. Particularly at a more refined level. Usually when we measure activity of enzymes or proteins, we expect that there is a temperature at which they are most efficient. Is this really the case for TSD species? I think it all comes back to the role of stochasticity in development and even evolution. Certain aspects of the environment are ALWAYS stochastic and unpredictable, and it seems likely that organisms would evolve the ability to operate better under these conditions than constant ones, which does make me wonder if there is still a most "efficient" temperature hidden outside of temperatures tested or if fluctuating temperatures are really better than any constant one. It seems there would be a significant cost to optimizing any biological process under unstable temperatures...

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  2. I like your take on TDSD! However, I wonder if you could reach a point where is too much fluctuation in temperature such as having too many cycles of cold to hot to cold in a day where you might see a decrease in size of hatchling success. When I was reading your paper, my mind went to climate change and how it might affect the temperature of eggs during certain developmental periods, and it would be cool to find out if having these higher temperatures at certain times may be more beneficial than harmful. I am also curious about the threshold of temperature which is beneficial at certain times and harmful at others such as is it in a 3 degree range or small, and does that change for each stage of development (such as going from a 3 degree range to 0.5 degree range)?

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