Exploiting genomic resources in studies of speciation and adaptive radiation of lizards in the genus Anolis

Lizards in the genus Anolis have radiated extensively within and among islands in the Caribbean. Here, I provide a prospectus for identifying genes underlying adaptive phenotypic traits in anoles. First I review patterns of diversification in Anolis and the important morphological axes along which divergence occurs. Then I discuss two features of anole diversification, the repeated, convergent evolution of ecomorphs, and phenotypic divergence among populations within species, that provide opportunities to identify genes underlying adaptive phenotypic variation. While small clutch size and difficulty with captive rearing currently limit the utility of quantitative trait locus analyses, comparative analyses of gene expression, and population genomic approaches are promising.     

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.     

Sexual dimorphism in traits related to locomotion: ontogenetic patterns of variation in Podarcis wall lizards

Sexual dimorphism in body size and shape in animals is normally linked to sexual selection mechanisms that modify the morphological properties of each sex. However, sexual dimorphism of ecologically relevant traits may be amplified by natural selection and result in the ecological segregation of both sexes. In the present study, we investigated patterns of sexual dimorphism of morphological traits relevant for locomotion in two lacertid lizards, Podarcis bocagei and Podarcis carbonelli, aiming to identify ontogenetic sources of variation. We analysed trunk and limb variation in relation to total body size, as well as the covariation of different traits, aiming to shed light on the proximate causation of adult sexual dimorphism. We find that, although immatures are generally monomorphic, adult females have a longer trunk, and adult males have longer fore and hind limbs. Both sexes differ substantially with respect to their growth trajectories and relationships between traits, whereas, in some cases, there are signs of morphological constraints delimiting the observed patterns. Because of the direct connection between limb size/shape and locomotor performance, which is relevant both for habitat use and escape from predators, the observed patterns of sexual dimorphism are expected to translate into ecological differences between both sexes. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 530–543.     

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

Abstract.— 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.     

Testing the island effect in adaptive radiation: rates and patterns of morphological diversification in Caribbean and mainland Anolis lizards

Many of the classic examples of adaptive radiation, including Caribbean Anolis lizards, are found on islands. However, Anolis also exhibits substantial species richness and ecomorphological disparity on mainland Central and South America. We compared patterns and rates of morphological evolution to investigate whether, in fact, island Anolis are exceptionally diverse relative to their mainland counterparts. Quite the contrary, we found that rates and extent of diversification were comparable--Anolis adaptive radiation is not an island phenomenon. However, mainland and Caribbean anoles occupy different parts of morphological space; in independent colonizations of both island and mainland habitats, island anoles have evolved shorter limbs and better-developed toe pads. These patterns suggest that the two areas are on different evolutionary trajectories. The ecological causes of these differences are unknown, but may relate to differences in predation or competition among mainland and island communities.     

Sexual selection versus alternative causes of sexual dimorphism in teiid lizards

Summary The presence and extent of sexual dimorphisms in body form (size and shape) of adult macroteiid lizards were investigated. Males were significantly larger than females in the temperate species, Cnemidophorus tigris, and in the tropical species, Ameiva ameiva and C. ocellifer. Young adult C. tigris males grew faster than young adult females within and between reproductive seasons. Adult males of all species had larger heads than adult females of the same body size; this difference increased with body size. Moreover, male C. tigris were heavier than females of the same snout-vent length. The causes and consequences of the sexual dimorphisms were also examined. The possible causes of body size are especially numerous, and distinguishing the relative influences of the various causal selection factors on body size is problematical. Nevertheless, observational field data were used to tentatively conclude that intrasexual selection was the cause of larger body size of C. tigris males relative to females because (1) larger males won in male aggressive interactions, (2) the winning males gained access to more females by repelling competitors and by female acceptance, (3) larger males consequently had higher reproductive success, and (4) other hypothetical causes of larger male size were unsupported.     

Physiological evolution during adaptive radiation: A test of the island effect in Anolis lizards

Phenotypic evolution is often exceptionally rapid on islands, resulting in numerous, ecologically diverse species. Although adaptive radiation proceeds along various phenotypic axes, the island effect of faster evolution has been mostly tested with regard to morphology. Here, we leveraged the physiological diversity and species richness of Anolis lizards to examine the evolutionary dynamics of three key traits: heat tolerance, body temperature, and cold tolerance. Contrary to expectation, we discovered slower heat tolerance evolution on islands. Additionally, island species evolve toward higher optimal body temperatures than mainland species. Higher optima and slower evolution in upper physiological limits are consistent with the Bogert effect, or evolutionary inertia due to thermoregulation. Correspondingly, body temperature is higher and more stable on islands than on the American mainland, despite similarity in thermal environments. Greater thermoregulation on islands may occur due to ecological release from competitors and predators compared to mainland environments. By reducing the costs of thermoregulation, ecological opportunity on islands may actually stymie, rather than hasten, physiological evolution. Our results emphasize that physiological diversity is an important axis of ecological differentiation in the adaptive radiation of anoles, and that behavior can impart distinct macroevolutionary footprints on physiological diversity on islands and continents.     

A comparative test of adaptive hypotheses for sexual size dimorphism in lizards

It is commonly argued that sexual size dimorphism (SSD) in lizards has evolved in response to two primary, nonexclusive processes: (1) sexual selection for large male size, which confers an advantage in intrasexual mate competition (intrasexual selection hypothesis), and (2) natural selection for large female size, which confers a fecundity advantage (fecundity advantage hypothesis). However, outside of several well-studied lizard genera, the empirical support for these hypotheses has not been examined with appropriate phylogenetic control. We conducted a comparative phylogenetic analysis to test these hypotheses using literature data from 497 lizard populations representing 302 species and 18 families. As predicted by the intrasexual selection hypothesis, male aggression and territoriality are correlated with SSD, but evolutionary shifts in these categorical variables each explain less than 2% of the inferred evolutionary change in SSD. We found stronger correlations between SSD and continuous estimates of intrasexual selection such as male to female home range ratio and female home range size. These results are consistent with the criticism that categorical variables may obscure much of the actual variation in intrasexual selection intensity needed to explain patterns in SSD. In accordance with the fecundity advantage hypothesis, SSD is correlated with clutch size, reproductive frequency, and reproductive mode (but not fecundity slope, reduced major axis estimator of fecundity slope, length of reproductive season, or latitude). However, evolutionary shifts in clutch size explain less than 8% of the associated change in SSD, which also varies significantly in the absence of evolutionary shifts in reproductive frequency and mode. A multiple regression model retained territoriality and clutch size as significant predictors of SSD, but only 16% of the variation in SSD is explained using these variables. Intrasexual selection for large male size and fecundity selection for large female size have undoubtedly helped to shape patterns of SSD across lizards, but the comparative data at present provide only weak support for these hypotheses as general explanations for SSD in this group. Future work would benefit from the consideration of alternatives to these traditional evolutionary hypotheses, and the elucidation of proximate mechanisms influencing growth and SSD within populations.     

Determinants of sexual differences in escape behavior in lizards of the genus Anolis: a comparative approach

Males and females are known to differ in a whole suite of characteristics,such as morphology, physiology, ecology, and behavior. Intersexualdifferences are generally believed to arise because of differencesin selective pressures on either sex. In this study, we investigatedwhether intersexual differences in escape behavior exist inlizards of the genus Anolis, and whether these could be explainedby intersexual differences in body size and/or microhabitatuse. To do so, we compared the behavioral response to an approachinghuman predator in the field in males and females of 12 Anolisspecies. We found that ecomorphs and sexes differ greatly withrespect to escape behavior. Twig anoles have the shortest approachdistance (i.e., distance between the observer and the lizardwhen it starts fleeing) and final distance (i.e., distance betweenthe observer and the lizard when it stops moving), comparedwith the other ecomorphs. The distance fled, on the contrary,is greatest in twig anoles. Also, females flee less soon andrun over shorter distances than do males. Since twig anolesare considered the most cryptic anoles, and females may be lessconspicuous than males, these results corroborate the idea thatwell camouflaged animals allow predators to come closer. Theinterspecific variation in sexual dimorphism in escape behavior,however, cannot be explained by the interspecific variationin sexual size dimorphism or sexual dimorphism in microhabitatuse. Thus, escape behavior appears determined by different factorsin males and females.     

Lack of convergence in aquatic Anolis lizards

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.     

Evolutionary assembly of island faunas reverses the classic island–mainland richness difference in Anolis lizards

Aim Islands are widely considered to be species depauperate relative to mainlands but, somewhat paradoxically, are also host to many striking adaptive radiations. Here, focusing on Anolis lizards, we investigate if cladogenetic processes can reconcile these observations by determining if in situ speciation can reduce, or even reverse, the classical island–mainland richness discrepancy. Location Caribbean islands and the Neotropical mainland. Methods We constructed range maps for 203 mainland anoles from museum records and evaluated whether geographical area could account for differences in species richness between island and mainland anole faunas. We compared the island species–area relationship with total mainland anole diversity and with the richness of island‐sized mainland areas. We evaluated the role of climate in the observed differences by using Bayesian model averaging to predict island richness based on the mainland climate–richness relationship. Lastly, we used a published phylogeny and stochastic mapping of ancestral states to determine if speciation rate was greater on islands, after accounting for differences in geographical area. Results Islands dominated by in situ speciation had, on average, significantly more species than similarly sized mainland regions, but islands where in situ speciation has not occurred were species depauperate relative to mainland areas. Results were similar at the scale of the entire mainland, although marginally non‐significant. These findings held even after accounting for climate. Speciation has not been faster on islands; instead, when extinction was assumed to be low, speciation rate varied consistently with geographical area. When extinction was high, there was some evidence that mainland speciation was faster than expected based on area. Main conclusions Our results indicate that evolutionary assembly of island faunas can reverse the general pattern of reduced species richness on islands relative to mainlands.     

Sexual dimorphism in chin shape: implications for adaptive hypotheses

The chin, or mentum osseum, is one of the most distinctive anatomical traits of modern humans. A variety of hypotheses for the adaptive value of the chin have been proposed, ranging from mechanical stress resistance to sexual selection via mate choice. While the sexual selection hypothesis predicts dimorphism in chin shape, most biomechanical hypotheses preclude it. Therefore determining the presence or absence of significant sexual dimorphism in chin shape provides a useful method for differentiating between various adaptive hypotheses; however, this has yet to be done due to a lack of quantitative data on chin shape. The goals of this study are therefore: (1) to introduce a new method for quantifying chin shape and (2) to determine the presence or absence of sexual dimorphism in chin shape in a diverse sample of modern humans. Samples were drawn from recent human skeletal collections representing nine geographic regions. Outlines of mentum osseum contours were quantified using elliptical Fourier function analysis (EFFA). Fourier coefficients were analyzed using principal components analysis (PCA). Sexual dimorphism in chin shape was assessed using PC loadings in the pooled geographic sample, and statistically significant differences were found. These findings provide the first quantitative, morphologically based evidence in support of adaptive hypotheses that predict dimorphism in chin shape, including the sexual selection hypothesis.     

Sexual dimorphism of the nymphal phase of ixodid tick species in the genus Dermacentor

In four studied Dermacentor species at preimaginal phases sexual dimorphism hardly reveals itself in body size and mass of individuals. The formation of sexual distinctions at the nymphal phase concerns different characters as in different species so in populations of one species. In D. niveus male and female nymphs differ in the length of II-III palpal joints and width of gnathosoma, in D. ushakovae in the length of scutum and its proportions, in the width of gnathosoma and hypostome and in the diameter of peritreme. The sex of D. silvarum nymphs can be identified by the width of gnathosoma, length of hypostome and diameter of peritreme. Female and male nymphs of D. marginatus from the Stavropol Territory and Armenia differ in the scutum proportions and populations from the western Pamirs in the length of scutum and gnathosoma.     

Macroecology and macroevolution of body size in Anolis lizards

Body size is one of the most influential traits affecting many ecological and physiological processes across animal and plant taxa. Studies of the environmental factors shaping body size patterns may evaluate either temporal or spatial dimensions. Here, we analyzed body size evolution in the radiation of Anolis lizards across both geographical and temporal dimensions. We used a set of macroecological and macroevolutionary methods to test current and past environmental effects on geographical gradients of body size and its evolutionary rates. First, we test whether a set of current ecological/physiological hypotheses (heat balance, productivity and seasonality) explains spatial body size gradients. Second, we evaluate how tempo (i.e. evolutionary rates) and mode (i.e. evolutionary process) of body size evolution changed through time and the role of paleo-temperatures on rates of body size evolution during the Cenozoic. We did not find a signature of current environmental variables driving spatial body size gradients. By contrast, we found strong support for a correlation between temperature changes (i.e. climate cooling) during the Cenozoic and rates of body size evolution (i.e. body size diversification). We suggest that patterns of body size evolution in Anolis lizards might be influenced by thermoregulatory behavior across clades and regions.     

Motion perception and visual signal design in Anolis lizards

Anolis lizards communicate with displays consisting of motion of the head and body. Early portions of long-distance displays require movements that are effective at eliciting the attention of potential receivers. We studied signal-motion efficacy using a two-dimensional visual-motion detection (2DMD) model consisting of a grid of correlation-type elementary motion detectors. This 2DMD model has been shown to accurately predict Anolis lizard behavioural response. We tested different patterns of artificially generated motion and found that an abrupt 0.3° shift of position in less than 100 ms is optimal. We quantified motion in displays of 25 individuals from five species. Four species employ near-optimal movement patterns. We tested displays of these species using the 2DMD model on scenes with and without moderate wind. Display movements can easily be detected, even in the presence of windblown vegetation. The fifth species does not typically use the most effective display movements and display movements cannot be discerned by the 2DMD model in the presence of windblown vegetation. A number of Anolis species use abrupt up-and-down head movements approximately 10 mm in amplitude in displays, and these movements appear to be extremely effective for stimulating the receiver visual system.     

Sexual dimorphism of tail length in lacertid lizards: test of a morphological constraint hypothesis

Males of many lizard species have longer tails than similarly-sized females. We hypothesized that this dimorphism is induced by a longer non-autotomous tail part in males, which is associated with the presence of the copulatory organs at the tail base, and presumably reduces the males' ability to escape predation by tail shedding. A compensatory mechanism would be an increase of total tail length in males, to achieve equal lengths of the autotomous tail part in both sexes. A critical prediction of this 'morphological constraint' hypothesis is that the extent of dimorphism in total tail length increases with the magnitude of sexual differences in length of the non-autotomous tail base. We tested this prediction through a comparative study in a small clade of lacertid lizards. Within each of nine species, sexual differences in length of the non-autotomous tail base and in total tail length do not change with body size. All species, except one, exhibit a clear male-biased dimorphism in length of the non-breakable tail base. In all species studied, males have longer tails than females. We used the method of phylogenetically independent contrasts to explore the interspecific relation between dimorphism in length of the tail base and sexual differences in total tail length. Contrary to our prediction, we found no evidence for a positive correlation between the extent of dimorphism in both traits. Thus, constraints imposed by the male copulatory organs on tail autotomy do not seem to be a significant factor in the evolution of dimorphism in tail length in this clade of lacertid lizards.