Anolis Species Research Articles

What is bred in the bone: Ecomorphological associations of pelvic girdle form in greater Antillean Anolis lizards.

Ecological niche partitioning of Anolis lizards of the Greater Antillean islands has been the focus of many comparative studies, and much is known about external morphological convergence that characterizes anole ecomorphs. Their internal anatomy, however, has rarely been explored in an ecomorphological context, and it remains unknown to what degree skeletal morphology tracks the diversity and ecological adaptation of these lizards. Herein, we employ CT scanning techniques to visualise the skeleton of the pelvic girdle in situ, and 3D geometric morphometrics to compare the form of the ilium, ischium, and pubis within and between ecomorphs. We examine 26 species of anoles representing four ecomorphs (trunk-ground, trunk-crown, crown-giant, twig) from three islands (Jamaica, Hispaniola, and Puerto Rico). The subtle variations in pelvic girdle morphology discovered are directly associable with all three parameters that we set out to focus on: phylogenetic relationship, specimen size, and assigned ecomorph category. Morphometric variation that correlates with size and/or phylogenetic signal varies between species and cannot be eliminated from the data set without markedly reducing its overall variability. The discovered patterns of skeletal variation are consistent with the demands of locomotor mechanics pertinent to the structural configuration of the microhabitat of three of the four ecomorphs, with the fourth having no discernible distinctive features. This manifests itself chiefly in the relative anteroposterior extent and anteroventral inclination of the ilium and pubis, which differ between ecomorphs and are postulated to reflect optimization of the direction of muscle vectors of the femoral protractors and retractors. Our investigation of the form of the pelvic girdle of anoles allows us to generalize our findings to entire ecomorph categories within a broad phylogenetic and biogeographic context. Differences in the form and configuration of the postcranial skeleton are directly related to ecological patterns.

Intraspecific Variation in the Information Content of an Ornament: Why Relative Dewlap Size Signals Bite Force in Some, But Not All Island Populations of Anolis sagrei.

In many animals, male secondary sexual traits advertise reliable information on fighting capacity in a male-male context. The iconic sexual signaling device of anole lizards, the dewlap, has been extensively studied in this respect. For several territorial anole species (experiencing strong intrasexual selection), there is evidence for a positive association between dewlap size and bite capacity, which is an important determinant of combat outcome in lizards. Intriguingly, earlier studies did not find this expected correlation (relative dewlap size-relative bite force) in the highly territorial brown anole lizard, Anolis sagrei. We hypothesize that the dewlap size-bite force relationship can differ among populations of the same species due to interpopulation variation in the degree of male-male competition. In line with this thought, we expect dewlap size to serve as a reliable predictor of bite performance only in those populations where the level of intrasexual selection is high. To tackle this hypothesis, we examined the relationship between male dewlap size and bite force on the intraspecific level in A. sagrei, using an extensive dataset encompassing information from 17 island populations distributed throughout the Caribbean. First, we assessed and compared the relationship between both variables in the 17 populations under study. Second, we linked the relative dewlap size-bite force relationship within each population to variation in the degree of intrasexual selection among populations, using sexual size dimorphism and dewlap display intensity as surrogate measures. Our results showed that absolute dewlap size is an excellent predictor of maximum bite force in nearly all A. sagrei populations. However, relative dewlap size is only an honest signal of bite performance in 4 out of the 17 populations. Surprisingly, the level of signal honesty did not correlate with the strength of intrasexual selection. We offer a number of conceptual and methodological explanations for this unexpected finding.

Thermal quality influences habitat use of two anole species

Regeneration of secondary forests on previously deforested or degraded land is one of the most dominant forms of land-use change in the tropics. However, the response of animal communities to forest regeneration is poorly understood. To evaluate support for thermal quality as a mechanism driving reptile species distributions during secondary forest succession, we measured operative temperatures and occupancy in three successional forest stages (pasture, secondary forest, and old growth forest) for two anole species common in the landscape (Norops humilis and Norops limifrons). We then measured thermal preference in laboratory experiments and used operative temperature and temperature preference measurements to determine how thermal quality of habitat changes over the course of secondary forest succession, and if occupancy varies as a function of thermal quality. We found that thermal quality was lowest in pasture habitat because of a large frequency of temperatures above the thermal preference range. However, in low thermal quality pasture sites, riparian habitats and remnant trees provided a thermal refuge for both lizard species. Our results support thermal quality as a mechanism for reptile species distributions in altered landscapes and highlight the importance of the maintenance of riparian corridors.

Herpetofauna of Cay Sal Bank, Bahamas and Phylogenetic Relationships of Anolis fairchildi, Anolis sagrei, and Tropidophis curtus from the Region

Although the terrestrial herpetofauna of the Bahamas Archipelago is largely well characterized, many smaller or outlying islands and island banks are poorly studied owing to their remoteness. The Cay Sal Bank is an uninhabited island bank lying between the Florida Keys and western Cuba. Politically a part of the Commonwealth of the Bahamas, the Cay Sal islands are disjunct from the rest of the Bahamas Archipelago to the east. The bank supports 117 small emergent islands around its perimeter, on which at least six species of squamates have been recorded. Recent expeditions have added to this species list, although several islands remain unsurveyed. Of these six squamate species, only Anolis fairchildi is considered endemic to the bank. The evolutionary relationships of the other species are speculated to derive from either Bahamian or Cuban progenitors. Here we report on a recent expedition to the Cay Sal Bank, and provide updated and novel island records. We further characterize the two native Anolis species and one Tropidophis species using molecular phylogenetic analyses to estimate the likely origins and divergence times of these species. We find that both Anolis species are recently (< 2 Mya) derived from, and likely conspecific with, west Cuban ancestors, whereas the Tropidophis is likely conspecific with the populations of Tropidophis curtus on the Great Bahamas Bank. Thus the terrestrial squamate herpetofauna on the bank are a product of dispersal from both the Great Bahamas Bank to the east and western Cuba to the south. We provide an updated understanding of the biogeography and evolutionary history of these squamates on the Cay Sal Bank.

Two new Andean species of Anolis lizard (Iguanidae: Dactyloinae) from southern Ecuador

ABSTRACTWe describe two new species of Anolis lizard that are sympatric on the Amazonian slopes of the Andes of southern Ecuador at elevations between 1440 and 1970 m. The new species may be distinguished from other Anolis by external anatomy, mitochondrial divergence and dewlap colour. We estimate the phylogenetic positions of the new species using Bayesian analysis of DNA sequence data including all species of Dactyloa-clade Anolis for which DNA data are available. Anolis hyacintogularis sp. nov. is sister to Anolis calimae, whereas Anolis lososi sp. nov. is sister to Anolis williamsmittermeierorum, herein reported for Ecuador for the first time. Individuals of both new species were collected within a protected area in southern Ecuador, Podocarpus National Park, which suggests that at least some populations of these species are well protected.www.zoobank.org/urn:lsid:zoobank.org:pub:E55FA804-E3FD-4412-8FEB-5234E29E272D

The evolution of androgen receptor expression and behavior in Anolis lizard forelimb muscles.

The motor systems that produce behavioral movements are among the primary targets for the action of steroid hormones, including androgens. Androgens such as testosterone bind to androgen receptors (AR) to induce physiological changes in the size, strength, and energetic capacity of skeletal muscles, which can directly influence the performance of behaviors in which those muscles are used. Because tissues differentially express AR, resulting in tissue-specific sensitivity to androgens, AR expression may be a major target of selection for the evolution of behavior. Anolis lizards (i.e., anoles) provide a robust system for the study of androgen-regulated traits, including the behavioral traits that facilitate social display and locomotion. In this study, we examined six anole species that demonstrate significant variation in the behavioral use of the forelimbs to measure the proportion of myonuclei in the bicep muscles that express AR. Using phylogenetic comparative analyses, we found that species with a greater proportion of nuclei positive for AR expression in the biceps exhibited greater frequencies of locomotor movements and pushup displays. These results suggest that AR expression in skeletal muscles may influence the evolution of androgen-regulated behaviors in this group.

The taxonomic and phylogenetic status of some poorly known Anolis species from the Andes of Colombia with the description of a nomen nudum taxon

We studied the phylogenetic status, morphological variation, dewlap color variation, and geographic distribution of four poorly known Anolis species nested in the Norops clade, particularly in the A. fuscoauratus group from the Andes of Colombia. In addition, we also describe a nomen nudum species based on morphological and molecular evidence. This nomen nudum taxa differ from other fuscoauratoids species in a combination of dewlap color, meristic traits, and molecular evidence. Our integrative analysis (molecular phylogenetics, morphology, and dewlap color) revealed the non-monophyletic status of these Andean taxa. We also confirmed the occurrence of A. fuscoauratus in the Magdalena valley in Colombia (a trans-Andean region). Our findings show that the evolution of Andean anoles is more complex than previously thought and more research is necessary to understand the diversity in this cryptic group.

Predictability in evolution: Adaptation of the Bonaire anole (Anolis bonairensis) to an extreme environment.

The extent to which evolution is deterministic (predictable), or random, is a fundamental question in evolution. This case study attempts to determine the extent to which interspecific divergence can be predicted from intraspecific trends related species. The mountainous Lesser Antilles are occupied by one or two anole species with very substantial intraspecific differences in the quantitative traits between xeric and rainforest habitats. These ecologically determined differences tend to be in parallel in each island species. A related species (Anolis bonairensis) lives on the far more xeric island of Bonaire, and this study tests the extent to which its interspecific divergence in hue and pattern traits can be predicted from the parallel intraspecific variation exhibited in Lesser Antillean anoles. Regression against a multivariate climate variable suggests that the hue and pattern of the Bonaire anole are consistently predicted from the ecologically determined intraspecific variation of its Lesser Antillean relatives. However, this predictability may be less consistent with other character systems, for example, scalation.

Substrate Availability and Selectivity Contribute To Microhabitat Specialization In Two Central American Semiaquatic Anoles

Both substrate availability and animal selectivity can contribute to patterns of animal substrate use. In the West Indies, where Anolis lizard ecomorphs are specialized for particular microhabitats, the relative influences of availability and selectivity on anole substrate use can change depending on the species and its location. Whether substrate availability and selectivity both contribute to microhabitat specialization in anoles outside the West Indies is largely unexplored. Two species of Central American semiaquatic anoles appear adapted for locomotion on different substrates—Anolis oxylophus on wood and leaves and Anolis aquaticus on rocks. I evaluated the contributions of substrate availability and selectivity to microhabitat specialization in these two species by comparing their substrate use to substrate availabilities in their stream macrohabitats. Both species selectively avoided the ground and perched instead on elevated substrates, yet the available elevated substrates differed between streams. Specifically, wood was most abundant in streams occupied by A. oxylophus, and rocks were most abundant in streams occupied by A. aquaticus. As is true with several West Indian anole ecomorphs, both substrate availability and selectivity contribute to microhabitat specialization in A. oxylophus and A. aquaticus.

Heteromorphism of “Homomorphic” Sex Chromosomes in Two Anole Species (Squamata, Dactyloidae) Revealed by Synaptonemal Complex Analysis

Iguanians (Pleurodonta) are one of the reptile lineages that, like birds and mammals, have sex chromosomes of ancient origin. In most iguanians these are microchromosomes, making a distinction between the X and Y as well as between homeologous sex chromosomes in other species difficult. Meiotic chromosome analysis may be used to elucidate their differentiation, because meiotic prophase chromosomes are longer and less condensed than metaphase chromosomes, and the homologues are paired with each other, revealing minor heteromorphisms. Using electron and fluorescent microscopy of surface spread synaptonemal complexes (SCs) and immunolocalization of the proteins of the SC (SYCP3), the centromere, and recombination nodules (MLH1), we examined sex chromosome synapsis and recombination in 2 species of anoles (Dactyloidae), Anolis carolinensis and Deiroptyx coelestinus, in which the sex chromosomes represent the ancestral condition of iguanians. We detected clear differences in size between the anole X and Y microchromosomes and found an interspecies difference in the localization of the pseudoautosomal region. Our results show that the apparent homomorphy of certain reptile sex chromosome systems can hide a cryptic differentiation, which potentially may influence the evolution of sexual dimorphism and speciation.

A Phylogenetic, Biogeographic, and Taxonomic study of all Extant Species of Anolis (Squamata; Iguanidae).

Anolis lizards (anoles) are textbook study organisms in evolution and ecology. Although several topics in evolutionary biology have been elucidated by the study of anoles, progress in some areas has been hampered by limited phylogenetic information on this group. Here, we present a phylogenetic analysis of all 379 extant species of Anolis, with new phylogenetic data for 139 species including new DNA data for 101 species. We use the resulting estimates as a basis for defining anole clade names under the principles of phylogenetic nomenclature and to examine the biogeographic history of anoles. Our new taxonomic treatment achieves the supposed advantages of recent subdivisions of anoles that employed ranked Linnaean-based nomenclature while avoiding the pitfalls of those approaches regarding artificial constraints imposed by ranks. Our biogeographic analyses demonstrate complexity in the dispersal history of anoles, including multiple crossings of the Isthmus of Panama, two invasions of the Caribbean, single invasions to Jamaica and Cuba, and a single evolutionary dispersal from the Caribbean to the mainland that resulted in substantial anole diversity. Our comprehensive phylogenetic estimate of anoles should prove useful for rigorous testing of many comparative evolutionary hypotheses. [Anoles; biogeography; lizards; Neotropics; phylogeny; taxonomy].

Condition dependence of shared traits differs between sympatric Anolis lizards.

In many species, sexually selected combat and display traits can confer dramatic fitness benefits to males by aiding in mate acquisition, so individuals maximally invest energy into their growth and maintenance. Such traits are deemed condition-dependent, as the energy that is available for investment depends on the health and condition of the individual. Condition dependence is present in a wide range of traits across many taxa, but the extent to which condition dependence varies among shared traits in closely related species is poorly understood. We tested for condition dependence in two Anolis lizards, the ground anole (Anolis humilis) and the slender anole (Anolis limifrons). Specifically, we measured dewlap area, jaw length, jaw width, and sprint speed, and then regressed one of two indices of body condition on each of these traits for both species. We found that dewlap area and jaw width exhibited condition dependence in ground anoles, but not in slender anoles. Sprint speed and jaw length were not condition-dependent in either species. The presence of condition dependence in ground anoles, but not slender anoles, implies evolutionary liability in the condition dependence of shared traits. Additionally, the fact that condition dependence was only detected in ground anoles, which have a greater relative dewlap size, suggests a potential role for signal evolution or strength of sexual selection in the evolution of condition dependence. Finally, our research suggests that variation in condition dependence of sexually selected traits could have implications for the evolution of dewlap diversity among Anolis species.

Does ecological specialization transcend scale? Habitat partitioning among individuals and species of Anolis lizards.

Ecological specialization is common across all levels of biological organization, raising the question of whether the evolution of specialization at one scale in a taxon is linked to specialization at other scales. Anolis lizards have diversified repeatedly along axes of habitat use, but it remains unknown if this diversification into habitat use specialists is underlain by individual specialization. From repeated observations of individuals in a population of Anolis sagrei in Florida, we show that the extent of habitat use specialization among individuals is comparable to the extent of specialization in the same traits among ten sympatric Anolis habitat specialist species in Cuba. However, the adaptive correlations between habitat use and morphology commonly seen across species of Anolis were not observed across individuals in the sampled population. Our results therefore suggest that while patterns of ecological specialization can transcend scale, these parallels are the consequence of distinct ecological processes acting at microevolutionary and macroevolutionary scales.

Comparative tests of the role of dewlap size in Anolis lizard speciation.

Phenotypic traits may be linked to speciation in two distinct ways: character values may influence the rate of speciation or diversification in the trait may be associated with speciation events. Traits involved in signal transmission, such as the dewlap of Anolis lizards, are often involved in the speciation process. The dewlap is an important visual signal with roles in species recognition and sexual selection, and dewlaps vary among species in relative size as well as colour and pattern. We compile a dataset of relative dewlap size digitized from photographs of 184 anole species from across the genus' geographical range. We use phylogenetic comparative methods to test two hypotheses: that larger dewlaps are associated with higher speciation rates, and that relative dewlap area diversifies according to a speciational model of evolution. We find no evidence of trait-dependent speciation, indicating that larger signals do not enhance any role the dewlap has in promoting speciation. Instead, we find a signal of mixed speciational and gradual trait evolution, with a particularly strong signal of speciational change in the dewlaps of mainland lineages. This indicates that dewlap size diversifies in association with the speciation process, suggesting that divergent selection may play a role in the macroevolution of this signalling trait.

Extreme thermal heterogeneity in structurally complex tropical rain forests

AbstractMost terrestrial species on Earth are ectothermic and track temperature at small spatial scales, from sun flecks to cool shaded spots. Current assessments of thermal heterogeneity in complex environments are predominately characterized by ambient temperature. This omission of solar radiation may lead to inaccurate conclusions regarding thermoregulation and distribution of species. We use thermal cameras to gather data on temperature heterogeneity in structurally complex rain forest environments. Using thermographic photographs, we capture the multidimensionality of climate created by vegetation by collecting over 76,000 temperature samples within approximately 1 m2 quadrats. The method was tested against three standard methods that record air temperature to determine possible omissions in capturing thermal heterogeneity in four geographic locations—Colombia, Borneo, Madagascar, and Australia. Across all locations, there was greater thermal heterogeneity in surface temperature than captured from ambient temperature technologies. Spatial variability in surface temperature on 1 d was greater than temporal variability of ambient temperature across the entire month, with extreme deviation from ambient temperatures. Importantly, when compared to the lower bounds for optimal performance for five tropical Anolis species, this technology captured thermal regimes that support the thermoregulatory needs of these species, whereas ambient air temperature methods suggested that these species would be in thermal debt. Sampling surface temperature at high resolutions across space in combination with intensive sampling of ambient temperature and informed spatial modeling should improve our understanding of the distribution of ectothermic species living within thermally heterogeneous environments.

A mid-Pleistocene rainforest corridor enabled synchronous invasions of the Atlantic Forest by Amazonian anole lizards.

Shifts in the geographic distribution of habitats over time can promote dispersal and vicariance, thereby influencing large-scale biogeographic patterns and ecological processes. An example is that of transient corridors of suitable habitat across disjunct but ecologically similar regions, which have been associated with climate change over time. Such connections likely played a role in the assembly of tropical communities, especially within the highly diverse Amazonian and Atlantic rainforests of South America. Although these forests are presently separated by open and dry ecosystems, paleoclimatic and phylogenetic evidence suggest that they have been transiently connected in the past. However, little is known about the timing, magnitude and the distribution of former forest connections. We employ sequence data at multiple loci from three codistributed arboreal lizards (Anolis punctatus, Anolis ortonii and Polychrus marmoratus) to infer the phylogenetic relationships among Amazonian and Atlantic Forest populations and to test alternative historical demographic scenarios of colonization and vicariance using coalescent simulations and approximate Bayesian computation (ABC). Data from the better-sampled Anolis species support colonization of the Atlantic Forest from eastern Amazonia. Hierarchical ABC indicates that the three species colonized the Atlantic Forest synchronously during the mid-Pleistocene. We find support of population bottlenecks associated with founder events in the two Anolis, but not in P.marmoratus, consistently with their distinct ecological tolerances. Our findings support that climatic fluctuations provided key opportunities for dispersal and forest colonization in eastern South America through the cessation of environmental barriers. Evidence of species-specific histories strengthens assertions that biological attributes play a role in responses to shared environmental change.

Does adaptive radiation of a host lineage promote ecological diversity of its bacterial communities? A test using gut microbiota of Anolis lizards.

Adaptive radiations provide unique opportunities to test whether and how recent ecological and evolutionary diversification of host species structures the composition of entire bacterial communities. We used 16S rRNA gene sequencing of faecal samples to test for differences in the gut microbiota of six species of Puerto Rican Anolis lizards characterized by the evolution of distinct 'ecomorphs' related to differences in habitat use. We found substantial variation in the composition of the microbiota within each species and ecomorph (trunk-crown, trunk-ground, grass-bush), but no differences in bacterial alpha diversity among species or ecomorphs. Beta diversity analyses revealed subtle but significant differences in bacterial composition related to host phylogeny and species, but these differences were not consistently associated with Anolis ecomorph. Comparison of a trunk-ground species from this clade (A.cristatellus) with a distantly related member of the same ecomorph class (A.sagrei) where the two species have been introduced and are now sympatric in Florida revealed pronounced differences in the alpha diversity and beta diversity of their microbiota despite their ecological similarity. Comparisons of these populations with allopatric conspecifics also revealed geographic differences in bacterial alpha diversity and beta diversity within each species. Finally, we observed high intraindividual variation over time and strong effects of a simplified laboratory diet on the microbiota of A.sagrei. Collectively, our results indicate that bacterial communities are only weakly shaped by the diversification of their lizard hosts due to the strikingly high levels of bacterial diversity and variation observed within Anolis species.

Evolutionary dynamics of Anolis sex chromosomes revealed by sequencing of flow sorting-derived microchromosome-specific DNA.

Squamate reptiles show a striking diversity in modes of sex determination, including both genetic (XY or ZW) and temperature-dependent sex determination systems. The genomes of only a handful of species have been sequenced, analyzed and assembled including the genome of Anolis carolinensis. Despite a high genome coverage, only macrochromosomes of A. carolinensis were assembled whereas the content of most microchromosomes remained unclear. Most of the Anolis species have homomorphic XY sex chromosome system. However, some species have large heteromorphic XY chromosomes (e.g., A. sagrei) and even multiple sex chromosomes systems (e.g. A. pogus), that were shown to be derived from fusions of the ancestral XY with microautosomes. We applied next generation sequencing of flow sorting-derived chromosome-specific DNA pools to characterize the content and composition of microchromosomes in A. carolinensis and A. sagrei. Comparative analysis of sequenced chromosome-specific DNA pools revealed that the A. sagrei XY sex chromosomes contain regions homologous to several microautosomes of A. carolinensis. We suggest that the sex chromosomes of A. sagrei are derived by fusions of the ancestral sex chromosome with three microautosomes and subsequent loss of some genetic content on the Y chromosome.

Discovery of a Giant Chameleon-Like Lizard (Anolis) on Hispaniola and Its Significance to Understanding Replicated Adaptive Radiations.

We report a new chameleon-like Anolis species from Hispaniola that is ecomorphologically similar to congeners found only on Cuba. Lizards from both clades possess short limbs and a short tail and utilize relatively narrow perches, leading us to recognize a novel example of ecomorphological matching among islands in the well-known Greater Antillean anole radiation. This discovery supports the hypothesis that the assembly of island faunas can be substantially deterministic and highlights the continued potential for basic discovery to reveal new insights in well-studied groups. Restricted to a threatened band of midelevation transitional forest near the border of the Dominican Republic and Haiti, this new species appears to be highly endangered.

Hemipenial morphology and diversity in South American anoles (Squamata: Dactyloidae)

Hemipenial morphology has provided useful characters to improve species identification and phylogenetic relationships in squamates. Here we provide hemipenial description and illustration of 13 South American anoles. At generic and specific levels, differences are mainly related to shape and ornamentation; intraspecific variation is low. An asulcate process, present in the hemipenis of most anole species studied, was highly variable among species and may be a useful taxonomic character in hemipenial morphology of this group.