Mountain passes are higher in the tropics – but maybe not if you can thermoregulate

Janzen vs. Bogert: How an evolutionary battle between environmental variation and behavioral regulation plays out in anoles

Divergent fields of biology are useful for providing alternative perspectives on a question, but the goal of integrative biology is to bring those ideas together to understand biological processes in new and innovative ways. It’s been 70 years in the making, but Munoz and colleagues have done just that. They link a hypothesis of physiological evolution presented by Bogert in 1949 (then more formally by Huey in 2003) with one of physiological performance by Janzen in 1967 to help us consider new insights into how animals might (or might not) evolve in the face of environmental change. To show support for this big idea, they look to a study system that has provided answers to big questions before, Caribbean anoles.

Though they may seem similar initially, these two hypotheses invoke two different viewpoints to understand physiological performance variation – that of either evolutionary or ecological processes. The Bogert effect proposes that, in ectotherms, the ability to modulate exposure to an environmental variable, such as temperature, might limit the effect that selection can have in driving evolution of physiological performance related to that trait. Seemingly independently, Janzen proposed that a narrow range of an environmental trait such as temperature would result in a similarly narrow physiological tolerance to that feature. Since tolerance limits can play a role in defining range limits, stable environments present a greater potential ecological barrier for organisms to cross.

Seeing both of these hypotheses side-by-side may make it seem obvious that they both play roles in facilitating and constraining thermal performance, but what is less obvious is how, exactly. What happens when an ectotherm with a specific and regulated preferred range of temperatures is exposed to a variable environment? Additionally, these hypotheses were developed by considering broad patterns, on the scales of elevational, latitudinal, and seasonal changes in temperature, but what if these same populations of behavioral regulators experience both stable and variable temperature regimes within the same habitat, such as with stable, lower nighttime vs. variable, higher daytime temperatures? Munoz and Bodensteiner take a clever, two-pronged approach to tease apart the role of each of these hypotheses on anole thermal performance.

Starting with Janzen’s hypothesis, they measured three performance traits of anoles from 7 species across 15 populations that spanned over 2400 m in elevation gain. Across this gradient, the nighttime temperatures were discrete and spatially and temporally homogeneous. However, the daytime temperatures overlapped and showed considerable variation both spatially and temporally. Whereas cold tolerance (CTmin) is important during the lower nighttime temperatures, preferred temperature (Tpref) and heat tolerance (CTmax) relate to behavioral and physiological performance during higher daytime temperatures. They found that, indeed CTmin matched the narrow bands of nighttime temperatures experienced at each elevation, but that there were no differences across populations or elevations in either of the other daytime-relevant variables. However, preferred temperature range and heat tolerance weren’t as broad as would be predicted by the range of daytime temperatures, suggesting these two traits may also have a narrow range that is regulated by movement across thermal microhabitats.

After finding support for the predictions derived from Janzen’s hypothesis for cold tolerance, Munoz and Bodensteiner then turned to testing the Bogert effect in these same populations by calculating the rate of evolution for each performance trait. If behavioral compensation shields traits from selection, then daytime-relevant traits would have slower rates of evolution than nighttime-relevant traits. Again their hypothesis was supported – cold tolerance evolves much faster than the other, regulated traits.

So how do animals adapt when they experience variation in abiotic traits but can also regulate their exposure to these traits? As we often conclude in biology, it depends. When the environment is stable (at night), behavioral buffering is irrelevant, ectothermic populations must conform, and strong selection on performance leads traits to match the environment, Janzen wins. However, when the environment is variable (during the day), behavioral buffering regulates and stabilizes performance traits, despite the variability of environmental traits. This misalignment weakens selection and slows trait evolution, Bogert wins. Additionally, traits can respond differently depending on how they relate to each of these circumstances.

After giving us a lot to think about with this insightful and well-supported synthesis of conceptual approaches, Munoz and Bodensteiner leave us with the challenge to now determine how these interactions play out in other organisms and across other physiological traits. So what do you say, who’s up for testing the Bogert-Janzen-Huey Hypothesis?

By Dr. Emily Kane

Emily is an Assistant Professor at Georgia Southern University. Her lab studies ecological and evolutionary biomechanics using fishes as model systems. Currently, they are use Trinidadian guppies to understand how local adaptation of feeding and swimming behaviors affects the ability to do both together during prey capture. Emily is also an advocate of outreach and science communication, incorporating these perspectives into both research and teaching.

https://www.thekanelab.com/

@KaneLabGSU

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