Anolis Species Research Articles

Determinants of spread in an urban landscape by an introduced lizard

Urban landscapes are a mixture of built structures, human-altered vegetation, and remnant semi-natural areas. The spatial arrangement of abiotic and biotic conditions resulting from urbanization doubtless influences the establishment and spread of non-native species in a city. We investigated the effects of habitat structure, thermal microclimates, and species coexistence on the spread of a non-native lizard (Anolis cristatellus) in the Miami metropolitan area of South Florida (USA). We used transect surveys to estimate lizard occurrence and abundance on trees and to measure vegetation characteristics, and we assessed forest cover and impervious surface using GIS. We sampled lizard body temperatures, habitat use, and relative abundance at multiple sites. At least one of five Anolis species occupied 79 % of the 1035 trees surveyed in primarily residential areas, and non-native A. cristatellus occupied 25 % of trees. Presence and abundance of A. cristatellus were strongly associated with forest patches, dense vegetation, and high canopy cover, which produced cooler microclimates suitable for this species. Presence of A. cristatellus was negatively associated with the ecologically similar non-native A. sagrei, resulting in reduced abundance and a shift in perch use of A. cristatellus. The limited spread of A. cristatellus in Miami over 35 years is due to the patchy, low-density distribution of wooded habitat, which limits dispersal by diffusion. The presence of congeners may also limit spread. Open habitats—some parks, yards and roadsides—contain few if any A. cristatellus, and colonization of isolated forest habitat appears to depend on human-mediated dispersal.

Dimorphism and divergence in island and mainland Anoles

Relative to the West Indies, the ecology and evolution of anoles inhabiting islands off Central and South America have received little attention. The paucity of studies on continental islands has limited our ability to generalize and extend results based on the West Indian paradigm, as well as our understanding of the profound differences between the adaptive radiations of continental vs. Greater Antillean anoles. Here we compare the morphological, ecological, behavioural and genetic divergence between Anolis nebulosus populations inhabiting a small island in the Bay of Chamela, Mexico, and a nearby mainland forest. Notably, the two populations exhibit intra-sexual dimorphism with respect to head and limb sizes, the first such polymorphism documented for an Anolis species. We also compare the shape of island and mainland A. nebulosus with each other, the six West Indian ecomorphs and a hypothetical generalist species. Finally, we address the generalist convergence hypothesis for anoles on single species islands. We conclude that convergence on a generalist morphology is widespread among solitary anoles in the West Indies. We present data on a limited sample of solitary anoles with mainland ancestors that suggest a parallel convergence on a similar generalist morphology, probably due to similar adaptive landscapes shaped by selective forces common to small island environments.

A revision of the green Anoles of Hispaniola with description of eight new species (Reptilia, Squamata, Dactyloidae)

We revise the species of green anoles (i.e., the species related to Anolis aliniger, A. chlorocyanus, and A. coelestinus) occuring on Hispaniola. Based on our analyses of morphological and molecular genetic data we recognize 16 species of green anoles, eight of which we describe as new species (A. apletolepis sp. nov., A. chlorodius sp. nov., A. divius sp. nov., A. eladioi sp. nov., A. gonavensis sp. nov., A. leucodera sp. nov., A. prasinorius sp. nov. and A. viridius sp. nov.) and three of which are raised from subspecific to species level (A. cyanostictus, A. demissus and A. pecuarius) and one is resurrected from synonymy with A. chlorocyanus (A. peynadoi). Because the six syntypes of A. chlorocyanus (MNHN 785, 787, 2007.2066–09) are conspecific with the only available syntype of A. coelestinus (i.e., MCZ 3347), we have petitioned the International Commission of Zoological Nomenclature (ICZN) to use its plenary power to set aside the type status of the syntypes of Anolis chlorocyanus and to allow the designation of a neotype in order to stabilize the current and long established usage of the names A. chlorocyanus and A. coelestinus. For each species we provide a standardized description of external morphology, color descriptions in life, color photographs in life, description and illustration of hemipenis morphology (if available), distribution maps based on the specimens examined, comments on the conservation status, and natural history notes. Finally, we provide a dichotomous key for the identification of the 16 species of green anoles occuring on Hispaniola.

A New Species of Phenacosaur Anolis (Squamata; Iguanidae) from Peru and a Comprehensive Phylogeny of Dactyloa-clade Anolis Based on New DNA Sequences and Morphology

We describe a new species of Anolis from the Andes of northern Peru. This form is similar to species formerly assigned to the genus Phenacosaurus and to Ernest Williams’ tigrinus series. That is, the new species possesses large smooth headscales, cryptic coloration, and short limbs and tail. We present new DNA and morphological data and perform a comprehensive phylogenetic analysis of the Dactyloa clade of Anolis. The new species is estimated to be close to phenotypically similar species from Peru and Venezuela. We revise the taxonomy of Dactyloa based on our estimate. Most previously recognized phylogenetically defined groups are retained with restricted species contents. Several species currently scorable only for morphological data could not be placed in any group with confidence. The species status of the enigmatic mainland form Anolis deltae should be re-examined with reference to the roquet group of southern Lesser Antillean Anolis.

Area, climate heterogeneity, and the response of climate niches to ecological opportunity in island radiations of Anolis lizards

AbstractAimRates of climate niche evolution underlie numerous fundamental ecological processes and patterns. However, while climate niche conservatism varies markedly among regions and clades, the source of this variation remains poorly understood. We tested whether ecological opportunity can stimulate radiation within climate niche space at biogeographic scales, predicting that rates of climate niche evolution will scale with geographic area and climate heterogeneity.LocationCaribbeanMethodsWe quantified two temperature axes (mean temperature and temperature seasonality of species' localities) of the climate niche for 130 Anolis species on Cuba, Hispaniola, Puerto Rico, Jamaica and the northern and southern Lesser Antilles. Using a species‐level phylogeny, we fitted macroevolutionary models that either constrained rates of climate niche evolution or allowed them to vary among regions. Next, we regressed region‐specific evolutionary rates against area, species richness and climate heterogeneity. We evaluated whether results were robust to uncertainty in phylogenetic and biogeographic reconstructions and the assumed mode of evolution.ResultsFor both niche axes, an Ornstein‐Uhlenbeck model that allowed the net rate of evolution (σ2) to vary among island groups fit the data considerably better than a single‐rate Brownian motion model. Nagelkerke pseudo‐R2 values of the fit of these OU models to mean temperature and seasonality axes were 0.43 and 0.66, respectively. Evolutionary rates for both axes were higher in larger areas, which also have more species. Only the rate of mean occupied temperature evolution was positively related to climate heterogeneity, and only after accounting for region size.ConclusionsRates of climate niche evolution scale consistently with the area available for radiation, but responses to climate heterogeneity vary among niche axes. For the mean temperature axis, climate heterogeneity generated additional opportunities for radiation, but for seasonality it did not. Overall, the physical setting in which a clade diversifies can influence where it falls on the evolutionary continuum, from climate niche conservatism to radiation.

Forelimb anatomy of three anole lizards: Anolis equestris , A. frenatus, and A. biporcatus

The genus Anolis is a model group for studying convergent evolution and adaptive radiations in vertebrates. Caribbean anoles have been classified into ecomorph categories, based on external morphology and position within the canopy, but less is known about mainland anoles. The goal of this study is to provide a detailed account of the forelimb in A. equestris, native to Cuba, and two mainland species, A. frenatus and A. biporcatus, and to analyze how these species compare to other anoles. For each species, external measurements were collected, muscles were dissected, photographed, and weighed and skeletal preparations were generated with Alizarin Red/Alcian Blue staining. External measurements indicate that A. equestris and A. frenatus are consistent with the Crown Giant ecomorph; whereas A. biporcatus is more consistent with Trunk-Crown ecomorphs. Dissections and skeletal preparations revealed similarities with existing accounts of anole species (A. sagrei and A. valencienni). However, differences were noted for biceps and flexor digitorum longus pars ulnaris (FDLU). Biceps pars profundus was present in A. equestris, A. frenatus, and A. biporcatus, while FDLU featured an additional tendon (to digit 1) in all three species and an additional tendon to digit 5 in A. frenatus. The greater number of tendons in these species may enhance grasping ability and stability while climbing.

Placing cryptic, recently extinct, or hypothesized taxa into an ultrametric phylogeny using continuous character data: a case study with the lizard Anolis roosevelti.

In recent years, enormous effort and investment has been put into assembling the tree of life: a phylogenetic history for all species on Earth. Overwhelmingly, this progress toward building an ever increasingly complete phylogeny of living things has been accomplished through sophisticated analysis of molecular data. In the modern genomic age, molecular genetic data have become very easy and inexpensive to obtain for many species. However, some lineages are poorly represented in or absent from tissue collections, or are unavailable for molecular analysis for other reasons such as restrictive biological sample export laws. Other species went extinct recently and are only available in formalin museum preparations or perhaps even as subfossils. In this brief communication we present a new method for placing cryptic, recently extinct, or hypothesized taxa into an ultrametric phylogeny of extant taxa using continuous character data. This method is based on a relatively simple modification of an established maximum likelihood (ML) method for phylogeny inference from continuous traits. We show that the method works well on simulated trees and data. We then apply it to the case of placing the Culebra Island Giant Anole (Anolis roosevelti) into a phylogeny of Caribbean anoles. Anolis roosevelti is a "crown-giant" ecomorph anole hypothesized to have once been found throughout the Spanish, United States, and British Virgin Islands, but that has not been encountered or collected since the 1930s. Although this species is widely thought to be closely related to the Puerto Rican giant anole, A. cuvieri, our ML method actually places A. roosevelti in a different part of the tree and closely related to a clade of morphologically similar species. We are unable, however, to reject a phylogenetic position for A. roosevelti that places it as sister taxon to A. cuvieri; although close relationship with the remainder of Puerto Rican anole species is strongly rejected by our method.

Multiple paths to aquatic specialisation in four species of Central American Anolis lizards

Aquatic anoles present an interesting ecomorphological puzzle. On the one hand, the link between habitat use and morphology is well established as convergent within the Caribbean anole radiation. On the other hand, aquatic anoles do not appear to form an ecomorphological group – rather, it appears that there may be several ways to adapt to aquatic habitats. We explore this issue by examining the ecology, morphology and performance of four species of Central American aquatic anoles belonging to two different lineages. Overall, we find that aquatic anoles overlap in multiple ecological and morphological dimensions. However, we do find some differences in substrate use, claw and limb morphology, and bite force that distinguish Anolis aquaticus from the other three species (A. lionotus, A. oxylophus and A. poecilopus). Our results suggest that A. aquaticus is adapted to climb on boulders, whereas the other species utilise vegetation in streamside habitats.

Phylogenetic relationships of Amazonian anole lizards (Dactyloa): Taxonomic implications, new insights about phenotypic evolution and the timing of diversification

The ecology and evolution of Caribbean anoles are well described, yet little is known about mainland anole species. Lack of phylogenetic information limits our knowledge about species boundaries, morphological evolution, and the biogeography of anoles in South America. To help fill this gap, we provide an updated molecular phylogeny of the Dactyloa (Dactyloidae), with emphasis on the punctata species group. By sampling understudied Amazonian taxa, we (i) assess the phylogenetic placement of the ‘odd anole’, D. dissimilis; (ii) infer the relationships of the proboscis-bearing D. phyllorhina, testing the hypothesis of independent nasal appendage evolution within the anole radiation; and (iii) examine genetic and dewlap color variation in D. punctata and D. philopunctata. Combining multiple nuclear loci with a review of the fossil record, we also (iv) estimate divergence times within the pleurodont iguanian clade of lizards, including Amazonian representatives of Dactyloa and Norops (Dactyloidae) and of Polychrus (Polychrotidae). We recover the five Dactyloa clades previously referred to as the aequatorialis, heteroderma, latifrons, punctata and roquet species groups, as well as a sixth clade composed of D. dissimilis and the non-Amazonian D. neblinina and D. calimae. We find D. phyllorhina to be nested within the punctata group, suggesting independent evolution of the anole proboscis. We consistently recover D. philopunctata nested within D. punctata, and report limited genetic divergence between distinct dewlap phenotypes. The most recent common ancestor of Dactyloa, Anolis and Norops dates back to the Eocene. Most Amazonian taxa within both Dactyloa and Norops diverged in the Miocene, but some diversification events were as old as the late Eocene and late Oligocene. Amazonian Polychrus diverged in the Pliocene. Our findings have broad implications for anole biogeography, disputing recent suggestions that modern dactyloid genera were present in the Caribbean region during the Cretaceous.

A revision of the Mexican Anolis (Reptilia, Squamata, Dactyloidae) from the Pacific versant west of the Isthmus de Tehuantepec in the states of Oaxaca, Guerrero, and Puebla, with the description of six new species.

We revise the species of anoles occurring along the Pacific versant of Mexico west of the Isthmus de Tehuantepec in the states of Oaxaca, Guerrero, and Puebla. Based on our analyses of morphological and molecular genetic data, we recognize 21 species, six of which we describe as new (i.e., Anolis carlliebi sp. nov., A. immaculogularis sp. nov., A. nietoi sp. nov., A. sacamecatensis sp. nov., A. stevepoei sp. nov., and A. zapotecorum sp. nov.). Furthermore, we synonymize Anolis forbesi Smith & Van Gelder 1955 with Anolis microlepidotus Davis 1954. Of the recognized species, six have smooth ventral scales (i.e., Anolis dunni, A. gadovii, A. liogaster, A. omiltemanus, A. peucephilus, and A. taylori) and 14 have keeled ventral scales (i.e., A. boulengerianus, A. carlliebi, A. immaculogularis, A. megapholidotus, A. microlepidotus, A. nebuloides, A. nebulosus, A. nietoi, A. quercorum, A. sacamecatensis, A. stevepoei, A. subocularis, A. unilobatus, and A. zapotecorum). In one species, A. macrinii, the ventral scales vary from smooth to weakly keeled. For each species we provide color descriptions in life, color photographs in life, descriptions and illustration of hemipenis morphology (if available), description of external morphology, distribution maps based on the specimensexamined, comments on the conservation status, and natural history notes. Finally, we provide a dichotomous key for the identification of the 21 species of anoles occurring along the Pacific versant of Mexico west of the Isthmus de Tehuantepec in the states of Oaxaca, Guerrero, and Puebla.

Functional morphology and comparative anatomy of appendicular musculature in Cuban Anolis lizards with different locomotor habits.

We examined the diversity of the musculoskeletal morphology in the limbs of Anolis lizards with different habitats and identified variations in functional and morphological adaptations to different ecologies or behaviors. Dissection and isolation of 40 muscles from the fore- and hindlimbs of five species of Anolis were performed, and the muscle mass and length of the moment arm were compared after body size effects were removed. Ecologically and behaviorally characteristic morphological differences were observed in several muscles. Well-developed hindlimb extensors were observed in ground-dwelling species, A. sagrei and A. bremeri, and were considered advantageous for running, whereas adept climber species possessed expanded femoral retractors for weight-bearing during climbing. Moreover, morphological variations were observed among arboreal species. Wider excursions of the forelimb joint characterized A. porcatus, presumably enabling branch-to-branch locomotion, while A. equestris and A. angusticeps possessed highly developed adductor muscles for grasping thick branches or twigs. These findings suggest divergent evolution of musculoskeletal characteristic in the limbs within the genus Anolis, with correlations observed among morphological traits, locomotor performance, and habitat uses.

The oestrogen pathway underlies the evolution of exaggerated male cranial shapes in Anolis lizards.

Sexual dimorphisms vary widely among species. This variation must arise through sex-specific evolutionary modifications to developmental processes. Anolis lizards vary extensively in their expression of cranial dimorphism. Compared with other Anolis species, members of the carolinensis clade have evolved relatively high levels of cranial dimorphism; males of this clade have exceptionally long faces relative to conspecific females. Developmentally, this facial length dimorphism arises through an evolutionarily novel, clade-specific strategy. Our analyses herein reveal that sex-specific regulation of the oestrogen pathway underlies evolution of this exaggerated male phenotype, rather than the androgen or insulin growth factor pathways that have long been considered the primary regulators of male-biased dimorphism among vertebrates. Our results suggest greater intricacy in the genetic mechanisms that underlie sexual dimorphisms than previously appreciated.

Phenotypic Plasticity in the Relative Hind-Limb Growth of Lab-RearedAnolis sagrei: Replication of Experimental Results and a Test of Perch Diameter Preference

Abstract Several observational and experimental studies have shown that perch diameter has an impact on the development of hind-limb length (HL) in Anolis species. This “phenotypic plasticity” in relative hind-limb growth (RHG) has implications for short-term and long-term adaptation to different structural habitats. Our study is the first to replicate research in which hatchling/juvenile Anolis sagrei were reared on narrow-diameter or broad-diameter dowels in a laboratory setting. Although subjects reared on different dowel diameters did not differ significantly in RHG at 5 weeks into the experiment, results at 15 weeks revealed a significant effect of treatment but not of sex: subjects in the broad (N = 69) treatment group exhibited significantly greater RHG than did subjects in the narrow (N = 61) treatment group. We extended this research with a novel follow-up study: we placed our lab-reared subjects into outdoor enclosures where they had a choice of narrow- or broad-diameter dowels on which to perch...

A new green anole lizard of the "Dactyloa" clade (Squamata: Dactyloidae) from the Magdalena river valley of Colombia.

We describe a new species of Anolis from the Magdalena river valley in Colombia. The new species is morphologically similar to Anolis ibanezi and A. chocorum, but differs in body and dewlap color, and head scalation. We performed an exploratory multivariate analysis based on 15 morphological characteristics of the new species and A chocorum and found that differences between both species are mainly associated with head dimensions. A phylogenetic analysis based on morphological characters suggests that the new species is nested within the "Dactyloa" clade of Anolis. Finally, we discuss phylogenetic relationships and biogeographical affinities based in its distribution.

Variation in steroid hormone levels among Caribbean Anolis lizards: Endocrine system convergence?

Variation in aggression among species can be due to a number of proximate and ultimate factors, leading to patterns of divergent and convergent evolution of behavior among even closely related species. Caribbean Anolis lizards are well known for their convergence in microhabitat use and morphology, but they also display marked convergence in social behavior and patterns of aggression. We studied 18 Anolis species across six ecomorphs on four different Caribbean islands to test four main hypotheses. We hypothesized that species differences in aggression would be due to species differences in circulating testosterone (T), a steroid hormone implicated in numerous studies across vertebrate taxa as a primary determinant of social behavior; more aggressive species were expected to have higher baseline concentrations of T and corticosterone. We further hypothesized that low-T species would increase T and corticosterone levels during a social challenge. Within three of the four island assemblages studied we found differences in T levels among species within an island that differ in aggression, but in the opposite pattern than predicted: more aggressive species had lower baseline T than the least aggressive species. The fourth island, Puerto Rico, showed the pattern of baseline T levels among species we predicted. There were no patterns of corticosterone levels among species or ecomorphs. One of the two species tested increased T in response to a social challenge, but neither species elevated corticosterone. Our results suggest that it is possible for similarities in aggression among closely related species to evolve via different proximate mechanisms.

Identification of sex‐specific molecular markers using restriction site‐associated DNA sequencing

A major barrier to evolutionary studies of sex determination and sex chromosomes has been a lack of information on the types of sex-determining mechanisms that occur among different species. This is particularly problematic in groups where most species lack visually heteromorphic sex chromosomes, such as fish, amphibians and reptiles, because cytogenetic analyses will fail to identify the sex chromosomes in these species. We describe the use of restriction site-associated DNA (RAD) sequencing, or RAD-seq, to identify sex-specific molecular markers and subsequently determine whether a species has male or female heterogamety. To test the accuracy of this technique, we examined the lizard Anolis carolinensis. We performed RAD-seq on seven male and ten female A. carolinensis and found one male-specific molecular marker. Anolis carolinensis has previously been shown to possess male heterogamety and the recently published A. carolinensis genome facilitated the characterization of the sex-specific RAD-seq marker. We validated the male specificity of the new marker using PCR on additional individuals and also found that it is conserved in some other Anolis species. We discuss the utility of using RAD-seq to identify sex-determining mechanisms in other species with cryptic or homomorphic sex chromosomes and the implications for the evolution of male heterogamety in Anolis.

Characters of external morphology used in Anolis taxonomy-definition of terms, advice on usage, and illustrated examples.

With the aim of establishing a reference for taxonomists, I describe and discuss characters of external morphology that have been used widely in descriptions of Anolis (sensu lato) species. For most characters, images are provided to illustrate the terms and definitions. Where appropriate, I give advice on how the counts and measurements should be done.

Conserved regulation of hoxc11 by pitx1 in Anolis lizards

Anolis lizards are an emerging model system for the study of limb development and evolution, but very little is known concerning the regulatory interactions that control limb patterning differences among Anolis species or what regulatory interactions are deeply conserved between Anolis and other tetrapod groups. Here we report the establishment of an embryonic limb micromass culture system that enables functional studies of forelimb and hindlimb gene regulatory networks in Anolis. Characterization of this culture system demonstrated that embryonic forelimb and hindlimb micromasses from different Anolis species are easy to sustain in culture for weeks, and the expression of forelimb and hindlimb-specific gene expression patterns are maintained for at least 8 days in culture. We tested the ability of this system to explore regulatory linkages between transcription factors and their putative target genes through the ectopic expression of a hindlimb-specific transcription factor, pitx1, in forelimb micromasses. We found that pitx1 expression in forelimb cells is sufficient to strongly induce the expression of hoxc11, a gene that normally exhibits hindlimb-restricted expression.

Anolis sex chromosomes are derived from a single ancestral pair.

To explain the frequency and distribution of heteromorphic sex chromosomes in the lizard genus Anolis, we compared the relative roles of sex chromosome conservation versus turnover of sex-determining mechanisms. We used model-based comparative methods to reconstruct karyotype evolution and the presence of heteromorphic sex chromosomes onto a newly generated Anolis phylogeny. We found that heteromorphic sex chromosomes evolved multiple times in the genus. Fluorescent in situ hybridization (FISH) of repetitive DNA showed variable rates of Y chromosome degeneration among Anolis species and identified previously undetected, homomorphic sex chromosomes in two species. We confirmed homology of sex chromosomes in the genus by performing FISH of an X-linked bacterial artificial chromosome (BAC) and quantitative PCR of X-linked genes in multiple Anolis species sampled across the phylogeny. Taken together, these results are consistent with long-term conservation of sex chromosomes in the group. Our results pave the way to address additional questions related to Anolis sex chromosome evolution and describe a conceptual framework that can be used to evaluate the origins and evolution of heteromorphic sex chromosomes in other clades.

Pattern of chromosomal changes in ‘beta’ Anolis (Norops group) (Squamata: Polychrotidae) depicted by an ancestral state analysis

BackgroundNeotropical lizards, genus Anolis (Polychrotidae), with nearly 380 species, are members of one of the most diversified genera among amniotes. Herein, we present an overview of chromosomal evolution in ‘beta’ Anolis (Norops group) as a baseline for future studies of the karyotypic evolution of anoles. We evaluated all available information concerning karyotypes of Norops, including original data on a recently described species, Anolis unilobatus. We used the phylogeny of Norops based on DNA sequence data to infer the main pattern of chromosomal evolution by means of an ancestral state analysis (ASR).ResultsWe identified 11 different karyotypes, of which 9 in the species had so far been used in molecular studies. The ASR indicated that a change in the number of microchromosomes was the first evolutionary step, followed by an increase in chromosome numbers, likely due to centric fissions of macrochromosomes. The ASR also showed that in nine species, heteromorphic sex chromosomes most probably originated from six independent events.ConclusionsWe observed an overall good correspondence of some characteristics of karyotypes and species relationships. Moreover, the clade seems prone to sex chromosome diversification, and the origins of five of these heteromorphic sex chromosome variants seem to be recent as they appear at the tip nodes in the ancestral character reconstruction. Karyotypic diversification in Norops provides an opportunity to test the chromosomal speciation models and is expected to be useful in studying relationships among anole species and in identifying cryptic taxa.