An Analysis of Inter-Population Divergence in Visual Display Behavior of the Green Anole Lizard (Anolis carolinensis)

Variation in habitat structure can profoundly affect the evolution of visual displays in animals. We compared the field display behavior of two populations of the green anole lizard (Anolis carolinensis) in Southern Louisiana. These two populations occupy habitats varying markedly in structure (clumped vs. continuous), ecological setting (urban vs. natural) and the degree of male competition and predation. We filmed 56 large adult male lizards during the active spring reproductive period and detected substantial divergence in display behavior between populations. We found that (1) relative dewlap areas did not differ significantly between populations, (2) Tulane anoles spent about twice as much time displaying compared with Good Hope field anoles, although the average display duration did not differ significantly between populations, and (3) the two populations differed significantly in the relative frequency of display types: lizards from the Tulane population used a higher proportion of A and B display types, whereas Good Hope Field anoles used C displays more often. Finally, we detected differences in other aspects of display behavior (use of display modifiers, volley length distributions). We suggest that these display differences may result from differences in green anole male density (three times higher at Tulane), combined with habitat differences (clumped vs. continuous).     

Assessment Strategies and the Effects of Fighting Experience on Future Contest Performance in the Green Anole (Anolis carolinensis)

Social experiences can be useful sources of information for animals charged with making fitness‐related decisions. Fighting experience can alter an animal's perception of its fighting ability possibly leading to changes in future contest decisions, which may increase/decrease their probability of winning future contests. Winner and loser effects have been revealed in a wide array of animals, but studies using reptilian models are rare. This study investigated the impact of fighting experience on future contest performance and outcome in the green anole lizard and investigated the assessment strategies used by anoles during contests of different intensities. To determine whether the green anole expresses winner or loser effects, focal animals engaged in a primary contest with a smaller (larger) opponent to gain a winning (losing) experience; opponent size asymmetries were a significant predictor of contest outcome. Focal individuals were isolated for 2 d before being given a secondary contest with a size‐matched, naïve opponent. We found no evidence of winner or loser effects 2 d following a previous contest. Although previous contest outcome did not dictate future contest success, dynamics of the previous contest did. Highly aggressive primary contest losers won a significant proportion of the secondary contests, while less aggressive losers were more apt to lose the secondary contest. Secondary contest success of prior winners was not influenced by earlier contest performance. Further analyses of contest dynamics reveal that individuals may use different assessment strategies depending on the intensity of the contest. Our results demonstrate that future contest success may be driven more by individual performance in a prior contest and less by prior contest outcome.     

No Evidence for Female Association with High-Performance males in the Green Anole Lizard, Anolis carolinensis

Sexual selection theory suggests that females may gain significant indirect fitness benefits from mating with males expressing good genes, particularly in animal species where the males provide no parental care. Whole‐organism performance abilities have previously been shown to enhance both survival and reproductive success in a range of taxa, and females who mate with high‐performance males might therefore gain significant indirect performance benefits. We tested the hypothesis that females associate preferentially with high‐performance males in the green anole lizard Anolis carolinensis in laboratory trials using multivariate statistical techniques. Our results indicate that male performance abilities do not influence female mating preferences, either in isolation or as a combined suite of traits. Thus, any indirect performance benefits that a female might gain for her offspring are likely not a result of a female choice process.     

Out of Florida: mtDNA reveals patterns of migration and Pleistocene range expansion of the Green Anole lizard (Anolis carolinensis)

Anolis carolinensis is an emerging model species and the sole member of its genus native to the United States. Considerable morphological and physiological variation has been described in the species, and the recent sequencing of its genome makes it an attractive system for studies of genome variation. To inform future studies of molecular and phenotypic variation within A. carolinensis, a rigorous account of intraspecific population structure and relatedness is needed. Here, we present the most extensive phylogeographic study of this species to date. Phylogenetic analyses of mitochondrial DNA sequence data support the previous hypothesis of a western Cuban origin of the species. We found five well‐supported, geographically distinct mitochondrial haplotype clades throughout the southeastern United States. Most Florida populations fall into one of three divergent clades, whereas the vast majority of populations outside Florida belong to a single, shallowly diverged clade. Genetic boundaries do not correspond to major rivers, but may reflect effects of Pleistocene glaciation events and the Appalachian Mountains on migration and expansion of the species. Phylogeographic signal should be examined using nuclear loci to complement these findings.     

Phosphodiesterase of Cone Photoreceptors from the Lizard, Anolis carolinensis

Cone and rod photoreceptors utilize cyclic guanosine monophosphate (cGMP) in the light regulation of membrane polarization. The prototype for visual transduction is established for rod photoreceptors, which utilize a cascade of reactions to regulate a cyclic nucleotide phosphodiesterase (PDE) (EC 3.1.4.17) and thereby control the intracellular concentration of cGMP. Although cones appear to utilize a comparable cGMP cascade for their phototransduction, evidence exists that the PDE from cone photoreceptors may be different from that of rods. Dissociated cone photoreceptors, isolated retinas, and cone outer segments from the lizard, Anolis carolinensis, have been used to identify and characterize a PDE enzyme complex that shares several features in common with the rod outer segment (ROS) PDE complex. Immunoadsorption and sodium dodecyl sulfate-polyacrylamide gel electrophoresis have identified a subunit of lizard cone PDE that has an apparent electrophoretic mobility of 84 kDa and a subunit of lizard rod PDE that migrates at approximately 90 kDa. The lizard cone PDE complex is similar in size, extraction, activation, and immunological characteristics to the PDE complex of rod photoreceptors from lizard, bovine, and human retinas. The lizard cone PDE complex, and perhaps that from cone photoreceptors in general, differs from that of ROS in its chromatographic properties on anion-exchange resins. The sharing of physical and activation properties of the rod and cone PDE complex is compatible with the phototransduction process occurring by a similar mechanism in both cell types. The differences in light sensitivity and speed of response may be attributable to features of the individual proteins that form the PDE complexes of rods and cones or to other undisclosed features of the respective cascades.     

Ethological Aspects of Stress in a Model Lizard, Anolis carolinensis

Research on the stress response in reptiles can provide a usefulcomparative perspective for understanding how the constituentelements of the response can be put into service of diversebehavioral adaptations. A summary of the neural and endocrinecauses and consequences of specific behavioral patterns seenin the small diurnal lizard, Anolis carolinensis, has provideda model for the exploration of the dynamics of autonomic andneurohormonal contributions to adaptive behavior. In this species,changes in body color provide indices of the flux of circulatingstress-relevant hormones, and are seen in situations from spontaneousexploration through agonistic behavior. Furthermore, captiveadult males spontaneously and consistently manifest social dominancerelationships that provide many of the elements of a stress-mediatedadaptive behavioral patterns. These patterns include suppressedreproduction and long-term coping apparently based more on stress-mediatedchanges in motivation than acquired changes in behavior.     

Identification and Comparative Analysis of the Protocadherin Cluster in a Reptile,the Green Anole Lizard

Background

The vertebrate protocadherins are a subfamily of cell adhesion molecules that are predominantly expressed in the nervous system and are believed to play an important role in establishing the complex neural network during animal development. Genes encoding these molecules are organized into a cluster in the genome. Comparative analysis of the protocadherin subcluster organization and gene arrangements in different vertebrates has provided interesting insights into the history of vertebrate genome evolution. Among tetrapods, protocadherin clusters have been fully characterized only in mammals. In this study, we report the identification and comparative analysis of the protocadherin cluster in a reptile, the green anole lizard (Anolis carolinensis).

Methodology/Principal Findings

We show that the anole protocadherin cluster spans over a megabase and encodes a total of 71 genes. The number of genes in the anole protocadherin cluster is significantly higher than that in the coelacanth (49 genes) and mammalian (54–59 genes) clusters. The anole protocadherin genes are organized into four subclusters: the δ, α, β and γ. This subcluster organization is identical to that of the coelacanth protocadherin cluster, but differs from the mammalian clusters which lack the δ subcluster. The gene number expansion in the anole protocadherin cluster is largely due to the extensive gene duplication in the γb subgroup. Similar to coelacanth and elephant shark protocadherin genes, the anole protocadherin genes have experienced a low frequency of gene conversion.

Conclusions/Significance

Our results suggest that similar to the protocadherin clusters in other vertebrates, the evolution of anole protocadherin cluster is driven mainly by lineage-specific gene duplications and degeneration. Our analysis also shows that loss of the protocadherin δ subcluster in the mammalian lineage occurred after the divergence of mammals and reptiles. We present a model for the evolutionary history of the protocadherin cluster in tetrapods.     

Ultrastructural studies of lizard (Anolis carolinensis) myogenesis in vitro

In vitro differentiation of lizard (Anolis carolinensis) skeletal muscle cells was studied by electron microscopy. Myogenesis was studied under conditions in which large numbers of postmitotic prefusion myoblasts accumulate (Growth Medium) and under conditions which are permissive for myotube formation (Fusion Medium). In Growth Medium, myogenic cells proliferate, then assume a characteristic spherical morphology which permits definitive identification of prefusion myoblasts. During the early stages of culture, these round myoblasts resemble myoblasts described in other systems; ultrastructural similarities and differences are discussed. After longer periods of culture in Growth Medium, a continuum of differentiation from isolated myofilaments to assembled myofibrils was seen in these mononucleated cells. These observations confirm the dissociability of contractile protein assembly and myoblast fusion Cultures maintained in Fusion Medium or transferred from Growth Medium to Fusion Medium form multinucleated myotubes on a predictable time scale. Myogenesis was followed in these cultures with particular reference to the early events in myofilament assembly and myofibril formation.     

The effects of diet on plasma and yolk steroids in lizards (Anolis carolinensis)

Steroids present in egg yolk have been shown to vary as a resultof numerous social and environmental influences and to produceboth positive and negative phenotypic outcomes in offspring.In the present study, we examined how quality of the diet affectsplasma and yolk steroids in the green anole (Anolis carolinensis),a lizard species with genotypic sex determination. We documentedthe effects of body condition on plasma testosterone (T) andcorticosterone (CORT)—steroids with frequently opposingeffects—in breeding females and on the T and CORT contentof their eggs. We chose to manipulate body condition via dietbecause resource availability is a relevant, fluctuating variablein the environment to which females can be expected to respond.Field-collected females were housed in the laboratory and kepton either a reduced, standard, or enhanced diet (differing innutritional quality and/or quantity) for ten weeks. Althoughfemales did not differ in body condition at the beginning ofthe study, we found these diet regimes effective in producingfemales that differed in condition by the end of the study.Females on diets of enhanced quality were in better condition,produced more, but not heavier, eggs, and had higher plasmaT concentrations than did females on a standard diet or oneof reduced quality. There was also a significant positive relationshipbetween laying sequence of eggs and yolk T for females on dietsof enhanced quality, but not for the females on diets of standardor reduced quality. There were no effects of quality of dieton CORT in plasma or yolk, but yolk T and yolk CORT exhibiteda strong positive correlation irrespective of treatment. Femaleson diets of reduced quality did not differ from females on standarddiets either with respect to reproductive output or to endocrineprofiles, in spite of being in worse body condition. These resultsdemonstrate that females’ body condition, physiology,and reproductive output can be manipulated by quality of diet,and that changes in deposition of yolk steroids in responseto diet may be minimal.     

A Neuroethological Study of Display Behavior in the Lizard Anolis Carolinensis (Reptilia, Lacertilia, Iguanidae)

A behavior inventory and ethogram for display behavior, an atlasof the principal forebrain nuclei and fiber tracts, and microtechniquesfor stereotaxic surgery were developed in conjunction with astudy of forebrain involvement in the display behavior of Anoliscarolinensis In a behavior inventory of 100 units consistingof states and events, forty-seven were observed exclusivelyor frequently in social situations. An analysis of the effectsof forebrain lesions on two stereotyped displays indicated involvementof the striatal area of the basal forebrain in species-typical"challenge" displays that are characteristic of territorialencounters between adult conspecifics. "Assertive" displaysassociated with elevated behavioral arousal were not significantlyaffected Lesions confined to the dorsal ventricular ridge resultedin no significant deficits in either display type.     

Effect of locomotor approach on feeding kinematics in the green anole (Anolis carolinensis)

Squamates are well-known models for studying to examine locomotor and feeding behaviors in tetrapods, but studies that integrate both behavioral activities remain scarce. Anolis lizards are a classical lineage to study the evolutionary relationships between locomotor behavior and complex structural features of the habitat. Here, we analyzed prey-capture behavior in one representative arboreal predator, Anolis carolinensis, to demonstrate the functional links between locomotor strategies and the kinematics of feeding. A. carolinensis uses two strategies to catch living insects on perches: Head-Up Capture and Jump Capture. In both cases, lizards use lingual prehension to capture the prey and the kinematic patterns of the trophic apparatus are not significantly influenced by the selected strategies. Therefore, to capture one prey type, movements of the trophic structures are highly fixed and A. carolinensis modulates the locomotor pattern to exploit the environment. Predation behavior in A. carolinensis integrates two different behavioral patterns: locomotor plasticity of prey-approach and biomechanical stereotypy of tongue prehension to successfully capture the prey.     

Display Behavior and Habitat Use in Single and Mixed Populations of Anolis carolinensis and Anolis sagrei Lizards

Introduced species can have a variety of effects on the behavior and ecology of native species. We compared display behavior and habitat use of introduced Anolis sagrei and native Anolis carolinensis lizards across three sites in Southern Louisiana. The chosen sites were similar in that they were all located in urban settings with clumped vegetation. The first site contained only A. sagrei, the second supported sympatric A. sagrei and A. carolinensis populations, and the third site harbored only A. carolinensis. We found that (1) A. carolinensis perched significantly higher when A. sagrei was present, consistent with previous studies, whereas perch height of A. sagrei was not altered by the presence of A. carolinensis; (2) A. carolinensis in single and mixed sites exhibited different proportions of display types, with individuals at the mixed Tulane site performing significantly more C displays than those at the single site; and (3) Anolis sagrei at the Tulane mixed site exhibited less push‐ups than those in the site with A. sagrei alone. These data suggest that the arrival of congeners can affect display behavior of anoles, although such effects are different for the natives and the invaders.     

Estrogen localization in the brain of the lizard, Anolis carolinensis (1)

Estrogen induces reproductive behavior in lizards by acting on specific areas of the brain. Neural areas that selectively concentrate radioactivity after 3-h-estradiol administration were mapped using thawmount autoradiography. Major accumulations of hormone-concentrating cells occur in the medial preoptic area, basal hypothalamus, amygdala (n. vetromedialis telencephali) and in and around the torus semicircularis. Numerous smaller accumulations are also described and the topographical distribution is compared with that of avian and mammalian species.     

Future social rank: forecasting status in the green anole (Anolis carolinensis)

Predicting the future social standing of an individual without aggressive social interaction may seem contradictory, as formation of social rank depends on agonistic interactions. In the lizard Anolis carolinensis, predicting social rank is possible using latency to eyespot formation (sympathetic darkening of postorbital skin from green to black during stressful agonistic interactions), because they form more rapidly in male lizards that become dominant. Darkened eyespots also inhibit aggressive behavior. As the timing of eyespot formation appears to be an important component of stress responsiveness and future social status, we hypothesized that a proactive disposition toward non-aggressive behavior, such as feeding and courtship, would be associated with aggressiveness. We assessed the relationship between rank and the temporal dynamics of eyespot formation, latencies to aggressive display, feeding, and reproductive behavior. Male lizards that became dominant were faster to respond to all types of stimuli tested (aggression, feeding, and courtship). The temporal dynamics of the neuroendocrine stress response appear to influence the motivation for behavioral response. Animals that recover from stress more quickly also eat, court, and fight more readily. In summary, this work suggests that latencies to aggressive, reproductive, and feeding behavior, as well as eyespot signals, are reliable predictors of future social status of individual male A. carolinensis.