Manuel Leal

Niche lability in the evolution of a Caribbean lizard community

Niche conservatism—the tendency for closely related species to be ecologically similar—is widespread. However, most studies compare closely related taxa that occur in allopatry; in sympatry, the stabilizing forces that promote niche conservatism, and thus inhibit niche shifts, may be countered by natural selection favouring ecological divergence to minimize the intensity of interspecific interactions. Consequently, the relative importance of niche conservatism versus niche divergence in determining community structure has received little attention. Here, we examine a tropical lizard community in which species have a long evolutionary history of ecological interaction. We find that evolutionary divergence overcomes niche conservatism: closely related species are no more ecologically similar than expected by random divergence and some distantly related species are ecologically similar, leading to a community in which the relationship between ecological similarity and phylogenetic relatedness is very weak. Despite this lack of niche conservatism, the ecological structuring of the community has a phylogenetic component: niche complementarity only occurs among distantly related species, which suggests that the strength of ecological interactions among species may be related to phylogeny, but it is not necessarily the most closely related species that interact most strongly.

Differences in Visual Signal Design and Detectability between Allopatric Populations of Anolis Lizards

We tested the prediction of the sensory drive hypothesis using four allopatric populations of the lizard Anolis cristatellus from two distinct environments (i.e., mesic and xeric conditions). For each population, we measured habitat light characteristics and quantified signal design by measuring the spectral and total reflectance and transmittance of the dewlap. We used these data to calculate dewlap detectability using an empirically based model of signal detection probability. We found that populations from mesic and xeric conditions occupy two distinct habitats with respect to light intensity and spectral quality and that dewlap design has diverged between populations in a way that increases signal detectability in each habitat. The major difference in dewlap design was in total reflectance and transmittance, making dewlaps from xeric habitats darker and dewlaps from mesic habitats brighter. Furthermore, dewlap detection decreased significantly when a dewlap from a xeric habitat is detected under the spectral conditions of a mesic habitat. The converse is true for a dewlap from a mesic habitat. We propose that sensory drive has promoted divergence in dewlap design in distinct habitat light conditions, and we discuss the possibility that selection might promote early stages of reproductive isolation as a by‐product of selection on dewlap design to distinct habitat light conditions.

Evidence for habitat partitioning based on adaptation to environmental light in a pair of sympatric lizard species

Terrestrial habitats exhibit a variety of light environments. If species exhibit evolutionary adaptations of their visual system or signals to habitat light conditions, then these conditions can directly influence the structure of communities. We evaluated habitat light characteristics and visual–signal design in a pair of sympatric species of lizards: Anolis cooki and Anolis cristatellus. We found that each species occupies a distinct microhabitat with respect to light intensity and spectral quality. We measured the relative retinal spectral sensitivity and found significant differences between the species that correlate with differences in habitat spectral quality. We measured the spectral reflectance of the dewlaps (colourful throat fans used in communication), and found that the A. cooki dewlap reflects little ultraviolet (UV), while that of A. cristatellus reflects strongly in the UV. For both species downwelling light (irradiance) is rich in UV. However the background light (radiance) is rich in UV for A. cooki, but low in UV for A. cristatellus. Thus, the dewlap of each species creates a high contrast with the background in the UV. Our findings strongly suggest that these two species are partitioning their habitat through specializations of the visual system and signal design to microhabitat light conditions.

Honest signalling during prey-predator interactions in the lizard Anolis cristatellus.

Current theory on the evolution of pursuit-deterrent signals predicts that it may be advantageous for the prey to communicate to the predator its alertness and its ability to escape an attack. I tested these predictions by staging predator-prey encounters between A. cristatellus lizards and a model of one of its predators under natural conditions. Results supported the use of pushup displays as pursuit-deterrent signals. The intensity of signals, measured as the number of pushups given during predation episodes, was significantly positively correlated with individual physiological condition measured as endurance capacity. Because endurance capacity can be a critical aspect limiting the ability of A. cristatellus to escape a predatory attack, pushup displays can potentially communicate an individuals ability to escape an attack and, therefore, can be categorized as honest signals. Furthermore, because pushup displays are widely used during anoline social interactions, predation pressure and sexual selection may simultaneously favour the evolution of honest communication to allow both the predator and the potential mate or male rival to assess individual quality using the same signal. Copyright 1999 The Association for the Study of Animal Behaviour.

Founder Effects Persist Despite Adaptive Differentiation: A Field Experiment with Lizards

Random and Directed Natural selection drives populations to adapt to new environments; the raw material or “founder effects” provided by the first colonizing individuals can thus have a formative influence on the populations future. Kolbe et al. (p. 1086, published online 2 February; see the cover) tested the relative contributions of selection and founder effects in Bahamian lizards. Founders were taken from an island covered in forest: These lizards had long hindlimbs for sprinting across the broad expanses of tree trunks. Long-limbed lizards were introduced to seven smaller islands covered in scrub that, before hurricane Frances in 2004 swept them away, had been populated by lizards with short hindlimbs better suited for navigating a twiggy habitat. After several generations, all the new lizard populations had adapted to their new habitats by evolving shorter hindlimbs but they also retained other morphological and genetic signatures from their founding ancestors. Thus, evolution occurs by a combination of arbitrary events, as well as those shaped by selection. Introduced populations of anoles retain characteristics of their founders and acquire adaptations to their new environment. The extent to which random processes such as founder events contribute to evolutionary divergence is a long-standing controversy in evolutionary biology. To determine the respective contributions of founder effects and natural selection, we conducted an experiment in which brown anole (Anolis sagrei) lizard populations were established on seven small islands in the Bahamas, from male-female pairs randomly drawn from the same large-island source. These founding events generated significant among-island genetic and morphological differences that persisted throughout the course of the experiment despite all populations adapting in the predicted direction—shorter hindlimbs—in response to the narrower vegetation on the small islands. Thus, using a replicated experiment in nature, we showed that both founder effects and natural selection jointly determine trait values in these populations.

Rapid change in the thermal tolerance of a tropical lizard.

The predominant view is that the thermal physiology of tropical ectotherms, including lizards, is not labile over ecological timescales. We used the recent introduction (∼35 years ago) of the Puerto Rican lizard Anolis cristatellus to Miami, Florida, to test this thermal rigidity hypothesis. We measured lower (critical thermal minimum [CTmin]) and upper (critical thermal maximum [CTmax]) thermal tolerances and found that the introduced population tolerates significantly colder temperatures (by ∼3°C) than does the Puerto Rican source population; however, CTmax did not differ. These results mirror the thermal regimes experienced by each population: Miami reaches colder ambient temperatures than Puerto Rico, but maximum ambient temperatures are similar. The differences in CTmin were observed even though lizards from both sites experienced nearly identical conditions for 49 days before CTmin measurement. Our results demonstrate that changes in thermal tolerance occurred relatively rapidly (∼35 generations), which strongly suggests that the thermal physiology of tropical lizards is more labile than previously proposed.

Behavioural flexibility and problem-solving in a tropical lizard

The role of behavioural flexibility in responding to new or changing environmental challenges is a central theme in cognitive ecology. Studies of behavioural flexibility have focused mostly on mammals and birds because theory predicts that behavioural flexibility is favoured in species or clades that exploit a diversity of habitats or food sources and/or have complex social structure, attributes not associated with ectothermic vertebrates. Here, we present the results of a series of experiments designed to test cognitive abilities across multiple cognitive modules in a tropical arboreal lizard: Anolis evermanni. This lizard shows behavioural flexibility across multiple cognitive tasks, including solving a novel motor task using multiple strategies and reversal learning, as well as rapid associative learning. This flexibility was unexpected because lizards are commonly believed to have limited cognitive abilities and highly stereotyped behaviour. Our findings indicate that the cognitive abilities of A. evermanni are comparable with those of some endothermic species that are recognized to be highly flexible, and strongly suggest a re-thinking of our understanding of the cognitive abilities of ectothermic tetrapods and of the factors favouring the evolution of behavioural flexibility.

Antipredator Responses of Anolis cristatellus (Sauria: Polychrotidae)

responses during encounters with its natural predatory snake Alsophis portoricensis: flight, immobility, body thrashing, biting, dewlapping, tail lashing, tonguebunch, head-bobbing, lateral body compression, lateral face-off, pushups, crouching, and tail autotomy. Alsophis portoricensis subduing time of Anolis cristatellus increased linearly with time the lizard spent biting the snake. Some of the behaviors (dewlapping, head-bobbing, lateral body compression, lateral face-off, pushups, and tongue-bunch) exhibited by A. cristatellus during predation episodes are also used by these lizards during social interactions. We propose, then, that all these behaviors be considered multipurpose behaviors of A. cristatellus.

LACK OF CONVERGENCE IN AQUATIC ANOLIS LIZARDS

Abstract Why convergent evolution occurs among some species occupying similar habitats but not among others is a question that has received surprisingly little attention. Caribbean Anolis lizards, known for their extensive convergent evolution among islands in the Greater Antilles, are an appropriate group with which to address this question. Despite the well-documented pattern of between-island convergence, some Greater Antillean anoles are not obviously part of the convergence syndrome. One example involves aquatic anoles—species that are found near to and readily enter streams—which have evolved independently twice in the Caribbean and also twice on mainland Central America. Despite being found in similar habitats, no previous study has investigated whether aquatic anoles represent yet another case of morphological convergence. We tested this hypothesis by collecting morphological data for seven aquatic anole species and 29 species from the six convergent types of Greater Antillean habitat specialists. We failed to find evidence for morphological convergence: the two Caribbean aquatic species are greatly dissimilar to each other and to the Central American species, which, however, may be convergent upon each other. We suggest two possible reasons for this lack of convergence in an otherwise highly convergent system: either there is more than one habitat type occupied by anoles in the proximity of water, or there is more than one way to adapt to a single aquatic habitat. We estimate that almost all of the 113 species of Greater Antillean anoles occupy habitats that are also used by distantly related species, but only 15% of these species are not morphologically similar to their distantly related ecological counterparts. Comparative data from other taxa would help enlighten the question of why the extent of convergence is so great in some lineages and not in others. Corresponding Editor: T. Smith

Habitat light and dewlap color diversity in four species of Puerto Rican anoline lizards

Closely related species often have signals that differ dramatically in design. The evolution of such differences may be important in the process of speciation. Selection for signal detectability under different habitat conditions has been proposed as a mechanism leading to the evolution of signal diversity. We examined dewlap color in four closely related species of Anolis lizards that occupy habitats with different light conditions. Initially, we tested the hypothesis that lizards choose specific light conditions within each habitat in which to signal. We rejected this hypothesis for all four species. We next calculated the detectability of the dewlap color of all four species at display locations in each habitat. If selection for detectability under the different light conditions explained the divergence in signal design, the occupant of a given habitat was predicted to have the highest signal detectability in that habitat. However, the rank order of detectability of the four dewlap colors was nearly the same in all four habitats. We concluded that divergent selection for signal detectability does not, by itself, explain the evolution of dewlap color diversity. We hypothesize that the evolution of dewlap color diversity results from simultaneous selection for multiple functions of dewlap color.