Scaredy-Cat Lizards Are The Product Of Their Environment

Natural selection shapes behavior as well as morphology — but it can have different effects in males and females!

by GrrlScientist for Forbes | @GrrlScientist

Assessment of risk-taking behaviors of the Bahaman brown anole (Anolis sagrei): Exploratory behavior is favored in the absence of predators, whereas avoidance of the ground is favored in their presence.
(Credit: Oriol Lapiedra / doi:
10.1126/science.aap9289)

Scientific research long ago established that natural selection can change an animal’s physical appearance. For example, animals with longer limbs are faster runners whereas animals with shorter limbs are more efficient climbers. But does natural selection shape an animal’s behavior, too?

This deceptively straightforward question has long been challenging to investigate scientifically, but thanks to an elegant new study that was published today in the journal, Science, the answer to that question is … yes. This study finds that risk-taking behavior in Bahama brown anoles is under natural selection pressure: in the absence of predators, the lizards were more adventurous but they were more cautious when predators were present.

Can natural selection act on behavior?

To unravel how behavior and adaptation affect each other, it’s important to understand how natural selection operates on an individual level within a given population (ref).

“Traditionally, scientists have viewed animal behavior as a somewhat idiosyncratic trait, with the perspective that behavior is an animal’s immediate response to its constantly-changing environment, and so behavior can’t be predicted,” said evolutionary biologist Michele Johnson, who studies evolution of lizard behavior at Trinity University, and who was not involved in the study.

But in the past 15 years or so, we’ve come to understand that animals often behave in predictable ways (ref), and that not all animals of a species behave in the same ways.

“In other words, animals have ‘personalities,’ or to use the jargon of the field, ‘behavioral syndromes’,” Professor Johnson said in email.

Although we know these behavioral differences have fitness consequences (i. e.; ref), “we don’t yet have a good idea for how natural selection acts on behavioral syndromes, or how these individual differences in behavior can evolve,” Professor Johnson elaborated in email.

To begin exploring this question, a team of researchers, led by comparative ecologist, Oriol Lapiedra, a postdoc at Harvard University, designed a series of experiments to study how the behavior of the Bahama brown anole, Anolis sagrei, is acted on by natural selection. This small plain lizard is a bit of a research superstar because it is very well-studied. It lives on islands throughout the Bahamas, and feeds on insects on or near the ground. The brown anole perches in vegetation to avoid predators whilst its main predator, the larger curly-tailed lizard, Leiocephalus carinatus, lives on the ground (Figure 1A).

Fig. 1. Assessment of risk-taking behavior and morphological characterization of A. sagrei individuals. (A) Anolis sagrei (left) and Leiocephalus carinatus (right) photographed on the experimental islands. (B) Experimental assessment of behavioral traits. Following, an A. sagrei individual was gently placed into a wooden refuge inside a butterfly cage. During a 3-min habituation period, we placed a clear plastic cage that contained a live adult L. carinatus between the refuge and a natural perch. Then, we remotely opened the door of the refuge and the A. sagrei individual was able to see the predator for 5 min. At the end of this period, we closed the door of the refuge and removed the plastic container with the L. carinatus from the experimental cage. After another 5-min habituation period, we again opened the refuge cover and measured the “time to initiation of exploration in a new environment”, defined as the time interval between the time we opened the refuge cover and the time when the lizard started exploring the experimental cage by poking its head out of the refuge. We defined “time exposed on the ground” as the interval between the “exposed time start” — defined as the time when the experimental lizard went out of the refuge (i.e., all its body, excluding the tail) — and the “exposed time end”, the time when the lizard either climbed the perch or hid underneath the rocks. © Example of an x-ray image from which we measured the morphological traits in this study (i.e., SVL and hindlimb length).
(doi:10.1126/science.aap9289)

The first thing that Dr. Lapiedra and his collaborators did was to assay differences in two behaviors shown by adult brown anoles: were the lizards cautious or were they risk-takers? The researchers measured this difference by placing individual brown anoles into a new environment where an individual predatory curly-tailed lizard was initially present in plain view of the anole (Figure 1B). After five minutes, the predator was removed and the door to the brown anole’s refuge was opened. The researchers measured (1) how quickly each brown anole began exploring, and (2) how long each exploring individual spent on the ground before climbing to safety or hiding under rocks. The premise was that individuals that explored new environments more quickly should survive better in the absence of terrestrial predators because they are more likely to find adequate insect food resources.

Dr. Lapiedra and his collaborators also measured morphological differences — limb length in this case — for all study anoles (Figure 1C). After all these measurements and assessments had been done, each lizard was randomly assigned to one of the eight islands, and before release onto their new island homes, they were given a subcutaneous electronic tag so each individual could be identified later. One week after the brown anoles had been released onto their new home, Dr. Lapiedra and his collaborators randomly added predatory curly-tailed lizards to four of the eight islands whilst the other four islands remained predator­-free tropical paradises.

Four months later, Dr. Lapiedra and his collaborators returned to their eight experimental islands and identified all surviving brown anoles from their tags. As expected, the researchers found that brown anole survival was lower on islands with predatory curly-tailed lizards than on the predator-free island paradises. They also found that brown anoles on islands with predators went to the ground less frequently, and their average perch height was more than twice as high as for brown anoles that lived on the predator-free islands.

Can a behavior that is adaptive in males be harmful in females?

Now here is where the fun begins. The Bahama brown anole is a sexually dimorphic lizard species where males and females differ in both morphology and behavior. Based on this, Dr. Lapiedra and his collaborators predicted that natural selection would act differently on the two sexes exposed to the different environmental conditions. Indeed, this is just what they found: natural selection favored adventurous females on predator-free islands (Figure 2A) whereas surviving females on islands with predators were less likely to spend time on the ground where they were exposed to danger (Figure 2B).

Fig. 2. Association between individual variation in behavior and survival of A. sagrei females after the 4-month experimental period. (Aand B) Time to initiation of exploration in a new environment (A) and time exposed on the ground (B) are represented separately for predator-free versus predator islands. Solid lines represent the fitted model logistic regression; dashed lines denote 95% confidence intervals. Dots represent individual values for both survivors (dots at top of each panel) and nonsurvivors (dots at bottom of each panel); darker dots are indicative of several individuals having similar values.
(doi:
10.1126/science.aap9289)

They found a greater negative effect by predatory curly-tailed lizards on female brown anoles who spent time on the ground, which is where their insect food is found. But surprisingly, male survival showed no effect at all (Figure 3A). Dr. Lapiedra and his team also found that female brown anoles used the ground less frequently than males did on islands with predators (11.9% versus 22.9%, respectively; Figure 3B).

Fig. 3. Comparison of survival frequencies and habitat use between sexes and experimental treatments. (A) The proportion of females surviving was higher on predator-free islands than on predator islands, but this difference was marginally nonsignificant for males. Error bars indicate SEM. (B) Both sexes used the ground less on predator islands, but this difference was greater for females than for males.
(doi:10.1126/science.aap9289)

Why were female brown anoles experiencing such a dramatically higher mortality rate than males on islands with predators? Dr. Lapiedra and his collaborators proposed that the female brown anoles were having more difficulties than males obtaining enough food on the predator islands. Indeed, four months after the experimental translocations, females on predator islands were in poorer body condition than females on predator-free islands — a pattern not seen for males. But why?

“We believe this could be explained by the fact that females, especially during the breeding season, need to visit to the ground more often because they need additional energy in order to lay eggs (which are also laid on the ground),” Dr. Lapiedra explained in email.

“So, their degree of exposure to predators may be higher in comparison to males.”

Is natural selection on behavior linked with morphology?

But was natural selection on behavior and morphology correlated? Specifically, are long-limbed anoles more likely to be risk takers? Because Dr. Lapiedra and his collaborators measured behavior and limb lengths in their study anoles before releasing them onto their experimental islands, they had some field data to contribute to this long-standing debate. They found that: (1) females used the ground more often on predator-free islands than on predator islands (Figure 3B) but surprisingly, relative hindlimb length did not affect survival on predator islands; (2) relative hindlimb length for males was not under selection pressure in either experimental treatment; (3) smaller bodied females survived better than larger females on predator islands; and finally, (4) selection on behavior and morphology was not correlated. So for females on predator-free islands, selection for longer hindlimbs was independent of selection for increased exploratory behavior, and for females on predator islands, selection for smaller body size was independent of selection for individuals that spent less time on the ground. These results indicate that selection on behavior and morphology can occur simultaneously — but in independent directions.

Natural selection can have dramatically different effects on behavior in males and females

“Their results are exciting because they show that selection acts on behavior in the ways we would predict, but at the same time, they show new patterns that we hadn’t considered before,” Professor Johnson said in email.

“I think this study is great because it demonstrates how selection is multi-faceted and can operate on multiple types of adaptive traits — in this case morphology and behaviour,” agreed evolutionary biologist Kiyoko Gotanda, an NSERC Banting Postdoctoral Fellow at the University of Cambridge, who was not involved in the study. “This is an experimental study in nature and as such, makes this an exciting step towards understanding the relative importance of behaviour in adaption.”

Equally interesting was seeing that natural selection acts differently on each sex.

“This result is evidence that natural selection is a complex process that shapes the behavior of males and females in different ways,” Dr. Lapiedra agreed.

But this would never have been discovered if this study hadn’t been designed to study each sex. As such, it is an essential example that “it is important to study both males and females, we should never assume that studying one of the sexes is enough to understand what happens at the population level.”

Source:

Oriol Lapiedra, Thomas W. Schoener, Manuel Leal, Jonathan B. Losos, and Jason J. Kolbe (2018). Predator-driven natural selection on risk-taking behavior in anole lizards, Science, 360(6392):1017–1020 | doi:10.1126/science.aap9289

Also cited:

Sasha R. X. Dall and Simon C. Griffith (2014). An empiricist guide to animal personality variation in ecology and evolution, Frontiers in Ecology and Evolution, 2:article 3 | doi:10.3389/fevo.2014.00003

Alison M. Bell, Shala J. Hankison, and Kate L. Laskowski (2009). The repeatability of behaviour: a meta-analysis, Animal Behaviour, 77(4):771–783 | doi:10.1016/j.anbehav.2008.12.022

Niels J. Dingemanse, Christiaan Both, Piet J. Drent, and Joost M. Tinbergen (2004). Fitness consequences of avian personalities in a fluctuating environment, Proceedings of the Royal Society of London B: Biological Sciences, 271(1541):847–852 | doi:10.1098/rspb.2004.2680


Originally published at Forbes on 31 May 2018.