Climate-mediated adaptation after mainland colonization of an ancestrally subtropical island lizard, Anolis carolinensis.

Climate-mediated evolution plays an integral role in species migration and range expansion. Gaining a clearer understanding of how climate affects demographic history and adaptation provides fundamental insight into the generation of intra- and interspecific diversity. In this study, we used the natural colonization of the green anole (Anolis carolinensis) from the island of Cuba to mainland North America to investigate the role of evolution at the niche, phenotypic and genetic levels after long-term establishment in a novel environment. The North American green anole occupies a broader range of thermal habitats than its Cuban sister species. We documented niche expansion in the mainland green anole, mediated primarily through adaptation to winter temperatures. Common garden experiments strongly suggest a genetic component to differences in thermal performance found between populations in different temperature regimes. Analysis of geographic variation in population structure based on 53 486 single nucleotide variants from RAD loci revealed increased genetic isolation between populations in different vs. similar thermal environments. Selection scans for environment-allele correlations reveal 19 genomic loci of known function that may have played a role in the physiological adaptation of A. carolinensis to temperate environments on the mainland.

Rapid evolution of a native species following invasion by a congener.

In recent years, biologists have increasingly recognized that evolutionary change can occur rapidly when natural selection is strong; thus, real-time studies of evolution can be used to test classic evolutionary hypotheses directly. One such hypothesis is that negative interactions between closely related species can drive phenotypic divergence. Such divergence is thought to be ubiquitous, though well-documented cases are surprisingly rare. On small islands in Florida, we found that the lizard Anolis carolinensis moved to higher perches following invasion by Anolis sagrei and, in response, adaptively evolved larger toepads after only 20 generations. These results illustrate that interspecific interactions between closely related species can drive evolutionary change on observable time scales.

Habitat use affects morphological diversification in dragon lizards.

Habitat use may lead to variation in diversity among evolutionary lineages because habitats differ in the variety of ways they allow for species to make a living. Here, we show that structural habitats contribute to differential diversification of limb and body form in dragon lizards (Agamidae). Based on phylogenetic analysis and ancestral state reconstructions for 90 species, we find that multiple lineages have independently adopted each of four habitat use types: rock-dwelling, terrestriality, semi-arboreality and arboreality. Given these reconstructions, we fit models of evolution to species' morphological trait values and find that rock-dwelling and arboreality limit diversification relative to terrestriality and semi-arboreality. Models preferred by Akaike information criterion infer slower rates of size and shape evolution in lineages inferred to occupy rocks and trees, and model-averaged rate estimates are slowest for these habitat types. These results suggest that ground-dwelling facilitates ecomorphological differentiation and that use of trees or rocks impedes diversification.

Nonlinear selection and the evolution of variances and covariances for continuous characters in an anole.

The pattern of genetic variances and covariances among characters, summarized in the additive genetic variance-covariance matrix, G, determines how a population will respond to linear natural selection. However, G itself also evolves in response to selection. In particular, we expect that, over time, G will evolve correspondence with the pattern of multivariate nonlinear natural selection. In this study, we substitute the phenotypic variance-covariance matrix (P) for G to determine if the pattern of multivariate nonlinear selection in a natural population of Anolis cristatellus, an arboreal lizard from Puerto Rico, has influenced the evolution of genetic variances and covariances in this species. Although results varied among our estimates of P and fitness, and among our analytic techniques, we find significant evidence for congruence between nonlinear selection and P, suggesting that natural selection may have influenced the evolution of genetic constraint in this species.

Evolutionary diversification of clades of squamate reptiles.

We analysed the diversification of squamate reptiles (7488 species) based on a new molecular phylogeny, and compared the results to similar estimates for passerine birds (5712 species). The number of species in each of 36 squamate lineages showed no evidence of phylogenetic conservatism. Compared with a random speciation-extinction process with parameters estimated from the size distribution of clades, the alethinophidian snakes (2600 species) were larger than expected and 13 clades, each having fewer than 20 species, were smaller than expected, indicating rate heterogeneity. From a lineage-through-time plot, we estimated that a provisional rate of lineage extinction (0.66 per Myr) was 94% of the rate of lineage splitting (0.70 per Myr). Diversification in squamate lineages was independent of their stem age, but strongly related to the area of the region within which they occur. Tropical vs. temperate latitude exerted a marginally significant influence on species richness. In comparison with passerine birds, squamates share several clade features, including: (1) independence of species richness and age; (2) lack of phylogenetic signal with respect to clade size; (3) general absence of exceptionally large clades; (4) over-representation of small clades; (5) influence of region size on clade size; and (6) similar rates of speciation and extinction. The evidence for both groups suggests that clade size has achieved long-term equilibrium, suggesting negative feedback of species richness on the rate of diversification.

The relationship between morphology, escape behaviour and microhabitat occupation in the lizard clade Liolaemus (Iguanidae: Tropidurinae: Liolaemini).

Phenotypic differences among species are known to have functional consequences that in turn allow species to use different habitats. However, the role of behaviour in this ecomorphological paradigm is not well defined. We investigated the relationship between morphology, ecology and escape behaviour among 25 species of the lizard clade Liolaemus in a phylogenetic framework. We demonstrate that the relationship between morphology and characteristics of habitat structure shows little or no association, consistent with a previous study on this group. However, a significant relationship was found between morphology and escape behaviour with the distance a lizard moved from a potential predator correlated with body width, axilla-groin length, and pelvis width. A significant relationship between escape behaviour and habitat structure occupation was found; lizards that occupied tree trunks and open ground ran longer distances from predators and were found greater distances from shelter. Behavioural strategies used by these lizards in open habitats appear to have made unnecessary the evolution of limb morphology that has occurred in other lizards from other clades that are found in open settings. Understanding differences in patterns of ecomorphological relationships among clades is an important component for studying adaptive diversification.

Natural restoration of the species-area relation for a lizard after a hurricane.

We document the decimation and recovery of the commonest lizard species, Anolis sagrei, on 66 islands in the Bahamas that were directly hit by Hurricane Floyd in September 1999. Before the hurricane, an island's area was a better predictor of the occurrence of A. sagrei than was its altitude. Immediately after, altitude was a better predictor: Apparently all lizards on islands lower than about 3 meters maximum elevation perished in the storm surge. After about 1 year, area again became the better predictor. By 19 months after the hurricane, A. sagrei populations occurred on 88% of the islands they formerly occupied. Recovery occurred via overwater colonization and propagation from eggs that survived inundation, mechanisms that were enhanced by larger island area. Thus, natural processes first destroyed and then quickly restored a highly regular species-area distribution.

Predators increase the risk of catastrophic extinction of prey populations.

There has been considerable research on both top-down effects and on disturbances in ecological communities; however, the interaction between the two, when the disturbance is catastrophic, has rarely been examined. Predators may increase the probability of prey extinction resulting from a catastrophic disturbance both by reducing prey population size and by changing ecological traits of prey individuals such as habitat characteristics in a way that increases the vulnerability of prey species to extinction. We show that a major hurricane in the Bahamas led to the extinction of lizard populations on most islands onto which a predator had been experimentally introduced, whereas no populations became extinct on control islands. Before the hurricane, the predator had reduced prey populations to about half of those on control islands. Two months after the hurricane, we found only recently hatched individuals--apparently lizards survived the inundating storm surge only as eggs. On predator-introduction islands, those hatchling populations were a smaller fraction of pre-hurricane populations than on control islands. Egg survival allowed rapid recovery of prey populations to pre-hurricane levels on all control islands but on only a third of predator-introduction islands--the other two-thirds lost their prey populations. Thus climatic disturbance compounded by predation brought prey populations to extinction.

Experimental studies of adaptive differentiation in Bahamian Anolis lizards.

Populations of the lizards Anolis carolinensis and A. sagrei were experimentally introduced onto small islands in the Bahamas. Less than 15 years after introduction, we investigated whether the populations had diverged and, if so, whether differentiation was related to island vegetational characteristics or propagule size. No effect of founding population size was evident, but differentiation of A. sagrei appears to have been adaptive, a direct relationship existed between how vegetationally different an experimental island was from the source island and how much the experimental population on that island had diverged morphologically. Populations of A. carolinensis had also diverged, but were too few for quantitative comparisons. A parallel exists between the divergence of experimental populations of A. sagrei and the adaptive radiation of Anolis lizards in the Greater Antilles; in both cases, relative hindlimb length and perch diameter are strongly correlated. This differentiation could have resulted from genetic change or environmentally-driven phenotypic plasticity. Laboratory studies on A. sagrei from a population in Florida indicate that hindlimb length exhibits adaptive phenotypic plasticity. Further studies are required to determine if the observed differences among the experimental populations are the result of such plasticity. Regardless of whether the differences result from plasticity, genetic change, or both, the observation that anole populations differentiate rapidly and adaptively when exposed to novel environmental conditions has important implications for understanding the adaptive radiation of Caribbean anoles.

Analysis of an evolutionary species-area relationship.

Large islands typically have more species than comparable smaller islands. Ecological theories, the most influential being the equilibrium theory of island biogeography, explain the species-area relationship as the outcome of the effect of area on immigration and extinction rates. However, these theories do not apply to taxa on land masses, including continents and large islands, that generate most of their species in situ. In this case, species-area relationships should be driven by higher speciation rates in larger areas, a theory that has never been quantitatively tested. Here we show that Anolis lizards on Caribbean islands meet several expectations of the evolutionary theory. Within-island speciation exceeds immigration as a source of new species on all islands larger than 3,000 km2, whereas speciation is rare on smaller islands. Above this threshold island size, the rate of species proliferation increases with island area, a process that results principally from the positive effects of area on speciation rate. Also as expected, the slope of the species-area relationship jumps sharply above the threshold. Although Anolis lizards have been present on large Caribbean islands for over 30 million years, there are indications that the current number of species still falls below the speciation-extinction equilibrium.

The relationship between sexual size dimorphism and habitat use in Greater Antillean Anolis lizards.

Sexual size dimorphism (SSD) is the evolutionary result of selection operating differently on the body sizes of males and females. Anolis lizard species of the Greater Antilles have been classified into ecomorph classes, largely on the basis of their structural habitat (perch height and diameter). We show that the major ecomorph classes differ in degree of SSD. At least two SSD classes are supported: high SSD (trunk-crown, trunk-ground) and low SSD (trunk, crown-giant, grass-bush, twig). Differences cannot be attributed to an allometric increase of SSD with body size or to a phylogenetic effect. A third explanation, that selective pressures on male and/or female body size vary among habitat types, is examined by evaluating expectations from the major relevant kinds of selective pressures. Although no one kind of selective pressure produces expectations consistent with all of the information, competition with respect to structural habitat and sexual selection pressures are more likely possibilities than competition with respect to prey size or optimal feeding pressures. The existence of habitat-specific sexual dimorphism suggests that adaptation of Anolis species to their environment is more complex than previously appreciated.

Evolutionary implications of phenotypic plasticity in the hindlimb of the lizard Anolis sagrei.

Species of Anolis lizards that use broad substrates have long legs, which provide enhanced maximal sprint speed, whereas species that use narrow surfaces have short legs, which permit careful movements. We raised hatchling A. sagrei in terraria provided with only broad or only narrow surfaces. At the end of the experiment, lizards in the broad treatment had relatively longer hindlimbs than lizards in the narrow treatment. These results indicate that not only is hindlimb length a plastic trait in these lizards, but that this plasticity leads to the production of phenotypes appropriate to particular environments. Comparison to hindlimb lengths of other Anolis species indicates that the range of plasticity is limited compared to the diversity shown throughout the anole radiation. Nonetheless, this plasticity potentially could have played an important role in the early stages of the Caribbean anole radiation.