THE BROWN ANOLE, a variety of lizard widespread in the Caribbean and southern United States, divides its time between the ground and the limbs of trees and shrubs. If a predator is around, the lizards are more likely to retreat into the greenery or hide in holes; a particularly intrepid lizard might take its chances and prowl the ground anyway. These differences in the animals’ behavior might affect whether they survive (and are selected by natural selection), argues a new paper in this week’s Science, co-authored by Oriol Lapiedra, a postdoctoral fellow in organismic and evolutionary biology, and Jonathan Losos, a longtime professor in the same department who recently moved to Washington University in St. Louis.
Whether and how behavior (or, more controversially, “personality”—the researchers avoid that term) plays a role in natural selection is a matter of some debate in biology, Losos explains. There are two broad perspectives: “One idea is that behavior impedes evolution. If species have some behavioral flexibility, then when conditions change they will alter their behavior in order to experience the same conditions. For example, in a warming world, lizards can just spend more time in the shade, and that would prevent them from needing to adapt to warmer temperatures,” he says. “The other idea is that behavior leads populations to expose themselves to new conditions, and evolve new features that adapt to those conditions. Like the idea of the first fish to crawl on land—that was a behavior, and once they did that that, it led to features that adapted them to land.”
“Usually, studies of behavior in natural selection are uncommon because behavior is more difficult to measure than morphology,” or an animal’s physical traits like size, Lapiedra says. “Behavior is usually more complicated.” The team captured 273 brown anoles in the Bahamas, and, to test how risk-taking each lizard was, Lapiedra placed them each in a wooden box or “refuge.” Across from them, in a clear plastic cage, sat a natural predator: the larger, imperious-looking curly-tailed lizard. The anoles peered at their predator through an opening in the refuge. Then, the curly-tailed lizard was removed, and the anoles were permitted to leave the box and explore their environment. The team measured how long it took each anole to leave its box, and how long they spent on the ground before jumping up onto a perch—using these indicators as proxies for risk-taking.
The anoles were then tagged and dispersed across eight tiny islands in the Bahamas, “so small,” Losos says, “that the official term for them is ‘rocks.’” The islands are regularly washed clean of lizards by hurricanes, he explains, so “they’re essentially the equivalent of test tubes.” On four of the islands, the researchers placed both the anoles and the curly-tailed lizards; the other, lucky half remained on predator-free islands. After four months, the animals were recaptured.
“What is particularly notable is that this is an experimental study in nature,” Losos says. “There have been other studies looking at behavioral variation and reproductive success, but to actually conduct an experiment in nature”—as opposed to in the lab—“on multiple populations is very rare.”
A test island in the Bahamas
Photograph by Oriol Lapiedra
Many more of the lizards survived, predictably, on predator-free islands; and on the predator islands, they spent much less time on the ground than high up in perches. On predator islands, Lapiedra says, “We would expect animals who spend more time on the ground to have more chances to be killed,” and that was what happened: on the predator-free islands, anoles that were more likely to explore their environment were more likely to survive; on the predator islands, anoles that spent less time on the ground were more likely to survive.
Curiously, the effects of risk-taking manifested only among female anoles—risk-taking males weren’t any more or less likely to survive. “That was very interesting to us,” Lapiedra says. “It suggests natural selection is a complex process that might be affecting only part of the population.” Losos adds, “We don’t have a particularly good explanation for it,” but some possibilities come to mind. Sexual dimorphism in the species is high, and males and females lead different lives: “Males are much more active and more visible than females, and spend a lot of their time displaying to each other and proclaiming, ‘This is my territory,’” he says. Males also have bright orange-red dewlaps that might make them perceptible to a predator; otherwise, the lizards’ brown skin blends in almost perfectly with branches. On the other hand, “Females have to lay their eggs in the ground, so that requires them to be on the ground in a way that males don’t have to be.”
Females were more likely to survive not just according to their behavior, but also their morphology: on predator-free islands, where the lizards spent more time on the ground, females with longer hind limbs that allowed them to run faster were more likely to survive. On predator islands, smaller females were more likely to survive. And on the predator islands, risk-aversion was a more important factor in survival than physical traits; on predator-free islands, the opposite was true. And the selection effects of behavior and morphology worked independently of each other: physical traits like limb size didn’t make the lizards more likely to take risks. That result, Losos says, suggests that the interaction between animals’ behavior and physical traits is more complicated than the theory has allowed: “Animal behavior and morphology can be selected on at the same time, and their relative strength depends on many conditions in the environment.”
The paper builds on Losos’s decades-long work on anoles, a group of lizards that are a common subject for the study of evolution because “there are 400 species of them, which is the largest genus of reptiles that exists,” he explains. “My career has been spent studying why this group is so diverse and how particular species adapt to the environment where they live.” His past research has shown that anoles move up to higher vegetation in the presence of predators, which provides the basis for the current study. The lizards, he says, are an ideal subject for scholars “who want to take a broad, integrative approach by studying different aspects of the same organism.”
Natural selection isn’t the same thing as evolution: the study suggests anoles were selected according to their risk-taking, but because the experiment took place within one generation, it’s too early to tell whether that behavior can be genetically transmitted. “A baby lizard that gets scared by a bird right after it hatches out of its egg might be risk-averse” for the rest of its life, Losos says. “You can have individual differences that might not be the result of genes, but of environment.” Lapiedra is now at work on studies of the offspring of the same anoles, to learn whether changes in risk-taking “are actually evolutionary, or whether they’re a consequence of plasticity in behavior.”
