All posts by Oriol Lapiedra

About Oriol Lapiedra

I am a postdoctoral fellow in the Losos lab at Harvard University. I am interested in understanding how the responses of animals to environmental changes affect their behavior, ecology and evolution.

Evolution 2017: Thermoregulation Simultaneously Impedes and Impels Evolution

Major Anole Annals contributor Martha Muñoz gave a brilliant talk at the Evolution meeting  as an awardee of a well-deserved ‘Young Investigator’ award from the American Society of Naturalists. In her talk, Muñoz discussed how two classic papers by Janzen (1967) and Huey et al. (2003) influenced the way she thinks about the interplay between behavior, physiology, and evolution. Not surprisingly, Anolis lizards played a leading role in her exposition.

2017-06-27 15.25.08

Martha Muñoz introduces the Cybotoid Anoles.

Martha’s talk, entitled “Janzen’s hypothesis meets the Bogert effect: a synthesis nearly 100 years in the making”, started by describing Janzen’s hypothesis. In short, Janzen (1967) predicted that physiological differences among populations across altitudinal bands would be stronger in tropical mountains than in temperate ones. The main argument was that populations can more easily adapt to a given temperature range in tropical environments because these ranges are stable throughout the year, whereas the temperatures of different altitudinal bands overlap more in temperate areas due to seasonal variation.

Martha explains how daytime and nighttime temperatures in the tropics mirror seasonal patterns in temperate and tropical climates.

Martha explains how day and night temperatures in the tropics mirror seasonal patterns in temperate and tropical climates.

Expanding on Janzen’s idea, Muñoz hypothesized that diurnal and nocturnal temperature variation in a single tropical mountain could also generate differences in physiological divergence among lowland and highland populations. The idea was that daytime temperatures were variable with overlap across elevation (similar to the seasonal picture in temperate areas) and nighttime temperatures were more constant and differed between elevations (similar to the seasonal picture in tropical areas).

To test this, Martha sampled populations in the Dominican Republic at sites ranging in elevation from sea level to 2400m. She then analyzed heat and cold tolerance of several species of anoles from the Anolis cybotes group. Results on cold tolerance (CT min) seem to agree with Janzen’s hypothesis: cold tolerance strongly covaries with altitude at night, with higher elevation populations having lower critical thermal minimums. Interestingly, however, heat tolerance (measured as CT max) was not at all associated with elevation.

Why did Janzen’s hypothesis fail to explain the evolution of heat tolerance across the altitudinal range? This question led to a key point of Muñoz’s talk: Janzen’s hypothesis might fail to predict evolution of CT max because it is agnostic about behavior. In the case of ‘cybotoid’ anoles, lizards from different altitudes could actively adjust their habitat use to achieve optimal temperatures. As a consequence, thermoregulatory behavior could forestall evolution of physiology in heat tolerance. By studying habitat use across different elevations, Muñoz showed that, although anoles behave as thermo-conformers at low elevations, they clearly thermoregulate at high elevations. In other words, anoles were at similar temperatures to the average available substrates in lowlands but their body temperatures were significantly higher than perches at higher elevation.

Martha explains how the thermoregulation can lead to slower evolution in a trait (the Bogert effect)

Martha explains how the thermoregulation can lead to slower evolution in a trait (the Bogert effect)

This was at least partially explained by habitat use differences: anoles at high elevations perched most frequently on boulders, which are on average about 5º C warmer than trees –the most used substrate in low altitudes. In fact, 90% of the trees Martha sampled at these high elevation sites were lower in temperature than the preferred temperature of the lizards! These data indicate that anoles from the A. cybotes group have buffered natural selection in physiology by means of behavioral adjustments –a phenomenon known as the Bogert effect (also called behavioral inertia; Bogert 1949).

Finally, the talk had a third part. And yes, it got even more interesting! Due to the observed habitat use differences in high latitudes, Muñoz and her collaborators predicted that although behavior could buffer physiological evolution on heat tolerance, it could spur evolutionary change in ecologically-relevant morphological traits (the behavioral drive hypothesis). Specifically, they predicted that increased use of boulders (for thermoregulation) at high elevations should drive morphological shifts in traits related to boulder use: head and limb morphology. They found evidence for these hypothesized morphological differences: high elevation lizards had higher head heights and longer hindlimb,  in agreement with functional predictions. Finally, a captive breeding experiment confirmed that these differences were the consequence of genetic changes and not simply due to developmental plasticity.

Martha’s research is a great example of how, as Huey said, studying behavior can be crucial to improve our understanding of evolutionary processes. We are looking forward to hear about future research from the Muñoz lab, which is about to open at Virginia Tech!


Janzen, D.H. 1967. Why mountain passes are higher in the tropics. American Naturalist 101:233–249

Huey, R.B., Hertz, P.E., Sinervo, B. 2003. Behavioral drive versus behavioral inertia in evolution: a null model approach. American Naturalist 161: 357–366.

Muñoz, M.M. et al. 2014b. Evolutionary stasis and lability in thermal physiology in a group of tropical lizards. Proc. R. Soc. B 281: 20132433.

Muñoz, M.M., Losos, J.B. Thermoregulation simultaneously promotes and forestalls evolution in a tropical lizard. (Accepted pending minor revision). American Naturalist.

Are Anoles Evolutionarily Adapting to Urban Habitats?

kristin winchell paper AA post

Photo by K. Winchell

In a global change scenario, the persistence of numerous animal populations is challenged by the consequences of human activities. Urbanization, for instance, represents a dramatic habitat transformation that has led to a general pattern of reduced biological diversity in these areas. Paradoxically, some species are doing very well in these new environments. This leads to the question of whether and how these populations are adapting to these new environmental conditions.

Although the number of studies providing evidence for phenotypic differences between urban and natural areas is growing fast, few studies have investigated whether and how animals might be evolutionarily adapting to the intensively modified urban habitats. Kristin Winchell and collaborators address this question in their recent publication in EvolutionPhenotypic shifts in urban areas in the tropical lizard Anolis cristatellus.” The authors studied the habitat use and morphology of forest vs. urban populations of Crested Anoles, Anolis cristatellus, from three municipalities in Puerto Rico. In short, this article provides evidence suggesting that urban anoles are under differential selective pressures as compared with those from forested habitats, and that these differences may have a genetic basis.

As the authors detail in their paper, anoles are a great system to study the morphological consequences of urbanization. This is because much information is available on the relationship between their habitat use, morphology and performance (reviewed in Losos 2009). In urban habitats, natural substrates have largely been replaced by artificial structures such as metal poles and walls. Consequently, it can be predicted that their performance on these surfaces is not optimal, as their morphology may not be suited to use these substrates. Indeed, it has been shown that lizards tend to perch on narrower, less smooth surfaces in natural habitats –a topic that has been dealt with in previous AA posts.

In this paper, the authors use field observations to show that lizards in urban areas use artificial substrates a large proportion of the time and that these urban substrates are broader and smoother than those in natural areas. Then, by X-raying lizards from the different habitats, the authors show that urban lizards have longer limbs (relative to their body size) and higher number of subdigital lamellae -which improve traction for perched lizards- than individuals from forested areas (Fig. 4). This is indeed consistent with ecomorphological predictions that anoles with longer limbs perform better on wider perches. Increased lamellae number should provide lizards with a better grip on smoother surfaces.

Fig. 4 from Winchell et al. (2016). This -really cool- figure shows how urban and natural populations differed in key morphological variables: (a) subdigital lamellae number and (b) limb length

Fig. 4 from Winchell et al. (2016). This -really cool- figure shows how urban and natural populations differed in key morphological variables: (a) subdigital lamellae number and (b) limb length

Finally, the authors conducted a common-garden rearing experiment in which they reared individuals from one of the three pairs of populations studied. The aim of this experiment was to rule out the possibility that morphological differences are merely the consequence of phenotypic plasticity. When measured at approximately one year of age, the first generation offspring of urban lizards showed longer forelimbs and more lamellae as compared to offspring of forest-dwelling lizards (Fig. 5). This result suggests that anoles in urban areas are under significantly different natural selection pressures and may be evolutionarily adapting to their human-modified environment.

Fig. 5 from Winchell et al (2016). Offspring reared in captivity showed the same trend as wild-caught populations of more subdigital lamellae and longer forelimbs in urban individuals: (a) relative limb length and (b) subdigital lamellae number

Fig. 5 from Winchell et al (2016). Offspring reared in captivity showed the same trend as wild-caught populations of more subdigital lamellae and longer forelimbs in urban individuals: (a) relative limb length and (b) subdigital lamellae number


Winchell, Kristin M., Reynolds, R. G., Prado-Irwin, Sofia R., Puente-Rolón, Alberto R., and Revel, Liam J. (2016). Phenotypic shifts in urban areas in the tropical lizard Anolis cristatellus.

Kolbe, J.J., Battles, A.C. & Avilés-Rodríguez. K. (2015) City slickers: poor performance does not deter Anolis lizards from using artificial substrates in human-modified habitats. Functional Ecology.

Losos, J.B. (2009) Lizards in an Evolutionary Tree: Ecology and Adaptive Radiation of Anoles. University of California Press, Berkeley, CA, USA.

Seasonality, Activity and Habitat Use of Insular and Mainland Populations of Anolis nebulosus

Seasonal fluctuations in the environment frequently lead to important modifications in the distribution of all kinds of resources in all sorts of ecosystems. Consequently, environmental seasonality has long been known to determine the biology, ecology and behavior of animals. Less known, however, is whether and how seasonality differentially affects populations of the same species inhabiting mainland and island areas.

By conducting field observations on  Anolis nebulosus from a mainland and a nearby island population in the Jalisco coast (Western Mexico), Siliceo-Cantero & Garcia (2015) investigated i) if anoles from these populations experienced similar degrees of seasonality and ii) whether they responded similarly to these seasonal changes. At each of the study sites, the authors conducted a series of transects at three different time blocks of the day within the normal activity range of the species. They collected information on each of the observed anoles including sex, perch height, temperature and humidity. Behavioral information was obtained for males by conducting focal observations in which researchers quantified movement rates, perch height and width, as well as the type of movements (i.e. dedicated to thermoregulation, socialization, and feeding).

Results showed several differences in substrate use and behavior between sexes, sites, and seasons. Overall, females perched lower than males (see Figure below), which could be a strategy of females to minimize competition with males. Interestingly, both sexes tended to perch lower on the mainland site. The authors suggest this could be a way of decreasing niche overlap with the larger lizard Sceloporus melanorhinus, a species that is not present on the island site. The reason why females perched lower during the rainy season whereas males did not remains unclear.

In general, males showed higher movement rates and covered longer distances on the San Agustin island site, maybe due to reduced environmental fluctuation on the island. The explanation for this is that, on the mainland, lizards may have to spend more energy to keep an appropriate body temperature so the costs of being active are higher that the potential benefits. Daily patterns of activity seem to be mainly determined by seasonal fluctuations in temperature and relative humidity (see Figure). The bimodal daily pattern of activity found during the dry season is possibly the consequence of an increased risk of overheating by direct solar irradiation, since the trees have lost their leaves during this time of the year. The lack of such bimodal pattern of activity on the island is compatible with possibility that this environment has less harsh weather conditions (e.g. lower temperatures due to regular wind currents), allowing anoles to be active with a lower risk of overheating.


Perch height differed among sexes, seasons and sites (means and 95% CI shown). Box shows significant differences among groups. Males (M), females (H), from island (I) and continent (C) during dry (S) and rainy (LI) seasons. (Figure 2 from Siliceo-Cantero & Garcia 2015)

In summary, the behavior of anoles is affected by seasonal fluctuations in their environment, but these effects seem to be the consequence of a complex interaction between several geographic and biotic factors. For instance, an increased seasonality in the environmental conditions of mainland may cause anoles to show a bimodal pattern of activity that does not exist on islands. In addition, the presence of a larger lizard is suggested to influence perch height in mainland anoles. Finally, increased intraspecific competition on islands could explain both increased activity of males (e.g. to defend their territories) as well as increased resource partition on perch height between males and females.