The Contronymic Effect of Behaviour on Evolution: Does Behaviour Promote or Retard Evolutionary Change?

Anolis shrevei on a rock. Photo courtesy of Katharina Wollenberg Valero.

Anolis shrevei on a rock. Photo courtesy of Katharina Wollenberg Valero.

Back when I was an undergrad, we were given the impression that animal behaviour and ecology (and evolution for that matter) were distinct disciplines. ‘Behaviour’ had its own classes, professors, and students, mostly separate from the ecologists. The disciplines also have their own, aptly named, journals: Animal Behaviour vs. Ecology. Of course, even then we knew that this division wasn’t a hard boundary and journals like The American Naturalist explicitly included ecology, behaviour and evolution, but we still didn’t think of these disciplines as inseparable. The impression seems to have stuck because fast forward 15 years and I was recently surprised when a colleague, upon hearing about our work on microhabitat use in agamids said, “I didn’t know you did behaviour.” Well, until that moment, I didn’t know I did either! I simply hadn’t thought about what we were doing in that way. Upon reflection, it should have been obvious, just like it should have been obvious that the behaviour/ecology distinction was a false one. I have no idea how widespread my once-perceived separation of ecology and behaviour is, but the fact that there’s a need for a journal, Behavioural Ecology, that specifically merges them suggests they’re still not perfectly integrated.

So why natter on about behaviour, ecology and evolution? Because a recent paper by Martha Muñoz and Jonathan Losos, published in The American Naturalist, is a fine example of why these shouldn’t be separated. Muñoz and Losos set up a dichotomy of hypotheses about how behaviour influences evolution: on the one hand, exploratory behaviour can expose species to novel selection pressures, stimulating evolution, but on the other, behavioural fidelity could shield species from those same selection pressures, ‘forestalling’ evolution. So, which is it? Well—spoiler alert—it’s both. So long nice dichotomy. To reach their findings, the authors looked at thermoregulatory behaviour and how it affects adaptation to high elevation habitats in the Anolis cybotes species group (specifically cybotes, armouri and shrevei). They found that, despite much cooler temperatures at higher elevations, high and low elevation species had selected temperatures in the lab and maintained similar body temperatures in the field, via increased thermoregulation at high elevations. Thus, despite the cooler temperatures, anoles hadn’t evolved to prefer colder temperatures on mountaintops. So behaviour halts evolution, right? Yes but no. To thermoregulate so extensively, anoles had to seek out warmer microhabitats, specifically boulders. And we know what happens when anoles change their perch type: evolution! Muñoz and Losos found that shrevei and armouri had flatter skulls, consistent with life on the rocks, as well as shorter hind limbs (but no differences in toe length or lamellae number). The evolutionary basis of the morphological change in head and femur traits was confirmed by a common garden. Nifty.

Effects of behavioral thermoregulation on evolution of high elevation anoles. On the left, thermal environment, body temperature and lab-selected-temperature of low and high elevation anoles. On the right, morphology of high and low elevation anoles in the field and in a common garden. Modified from Figs 1 and 2 in Muñoz and Losos (2017).

Effects of behavioral thermoregulation on evolution of high elevation anoles. On the left, thermal environment, body temperature and lab-selected-temperature of low and high elevation anoles. On the right, morphology of high and low elevation anoles in the field and in a common garden. Modified from Figs 1 and 2 in Muñoz and Losos (2018).

The overall message of the paper is clear: the same behaviour inhibited evolution along one niche axis and promoted it along another. Muñoz and Losos argue that the lack of evolutionary change in thermal traits arises from the Bogert effect, where behaviour limits exposure to novel selection pressures. However, there is a chance that the lack of evolution could be due to other constraints, like a lack of genetic variation. Testing this would require an experiment with a control group of lizards that couldn’t behaviourally avoid thermal selection pressures. A previous paper by Muñoz, Losos and others, provided just such a natural experiment. In that study, Muñoz et al. found that lower CTmin has evolved in high elevation cybotoids, relative to low elevation ones. Why? Because at night, when its coldest, anoles are unable to behaviourally thermoregulate to avoid the cold –voilà, a control where the Bogert effect was negated. And once behaviour was removed from the equation? Evolution! This finding adds even more weight to the role of behaviour in inhibiting the evolution of thermal traits in this system. Cool stuff (I make no apologies for that pun).

There’s lots more in the Muñoz and Losos paper than I touched on here so give it a thorough read. It goes a long way to destroying any divisions that might still exist between behaviour, ecology and evolution and it makes a strong case for why we need to consider multiple niche dimensions when we talk about niche evolution and conservatism. Plus, it gave me an excuse to use the word ‘contronymic.’

Muñoz, M.M. & Losos, J.B. 2018. Thermoregulatory behavior simultaneously promotes and forestalls evolution in a tropical lizard. The American Naturalist. DOI:10.1086/694779.

About Adam Algar

Associate Professor at the University of Nottingham (UK). My research focuses on niche limits and dynamics across scales, from individual organisms to the globe. Mostly lizards.

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