Intraspecific correlations among morphology, performance and habitat use within a green anole lizard (Anolis carolinensis) population

We examined habitat use, morphology, jumping and clinging ability for 403 juvenile, female and male green anole lizards, Anolis carolinensis, in a population in south‐eastern Louisiana. We sought to answer three questions: (1) Do age/sex classes differ in habitat use, morphology and performance ability? (2) Do habitat use, morphology and performance correlate among all individuals across three age/sex classes (juveniles, females and males)? (3) Do juveniles compensate for their poor absolute performance capacities by being better performers on a relative scale? The three age/sex classes were found to differ significantly in size‐adjusted morphology, habitat use and size‐adjusted performance capacity. Juveniles tended to occupy perches which were closer together than those of adult males and females. The distal elements of the hindlimb (femur, tibia) were significantly longer in males than in females and juveniles, while females were more stocky than males and juveniles. The only significant overall ecomorphological relationship detected was between the lengths of the distal hindlimb elements and maximum jump acceleration. Our hypothesis that juveniles should be better performers (relative to size) compared to adults was disproved, as adult females were always the best performers relative to size. Our analysis of a mainland anole population presents a different view of population structure compared to similar studies involving Caribbean Anolis lizards, which show more ecological differentiation among age/sex classes, and also show that juveniles are relatively good performers. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85 , 211–221.     

Evolutionary correlations among morphology, habitat use and clinging performance in Caribbean Anolis lizards

A central issue in evolutionary biology concerns whether morphology, performance and habitat use have coevolved. We investigated evolutionary relationships among the size of the subdigital toepad, clinging ability and perch height in 12 species of Caribbean Anolis lizard. Specifically, we predicted that: (1) because larger anole species tend to perch high in the canopy, both toepad area and clinging ability should scale with positive allometry to enable small and large lizards to possess approximately similar ratios of both variables relative to mass; (2) anole species with relatively larger toepads (i.e. size-adjusted) should be relatively better clingers compared with species with relatively small toepads; (3) species that perch high in the canopy should possess relatively large clinging abilities (either on an absolute or a size-adjusted basis). Our first hypothesis was refuted, as both toepad area and clinging ability scaled close to isometry (0.67) relative to mass, indicating that large lizard species have low ratios of clinging ability to mass compared with small lizard species. However, our second and third predictions were confirmed. Anole species with relatively larger toepads were relatively better clingers compared with species with relatively smaller toepads. Anole species that perched high in the canopy (either on an absolute scale or relative to size) tended to have relatively larger toepads and greater clinging capacities compared with species that perched lower in the canopy. These data provide indirect comparative evidence that the evolution of increased toepad size in some anole species is adaptive, by facilitating the occupation of perches high in the canopy.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 389–398.     

Relationships among morphology, clinging performance and habitat use in Liolaemini lizards

The central tenet of ecomorphological theory holds that different ecological requirements lead to different organismal designs (morphology). Here, we studied the relationships between performance (interlocking grasping) and forelimb morphological traits in species of lizards that exploit different structural habitats in a phylogenetic context. The performance (measured by the maximum force of clinging to substrate) was measured on different substrate types. After phylogenetically informed analyses, we found that arboreal and saxicolous species showed stronger resistance to mechanical traction in all substrates when compared to generalists and sand dweller lizards. These species showed a positive relationship between forelimb dimensions (humerus length and length of claw of toe 5) and maximum force exerted, on the contrary, hand width, claw height (CH) of digits III and IV and claw length of toe 4 showed a negative relationship. In addition, we observed a partial positive correlation between CH and maximal cling force on rough surfaces, but not on smooth surfaces.     

Hormones, sexual signals, and performance of green anole lizards (Anolis carolinensis)

The evolutionary processes that result in reliable links between male signals and fighting capacity have received a great deal of attention, but the proximate mechanisms underlying such connections remain understudied. We studied a large sample of male green anole lizards (Anolis carolinensis) to determine whether testosterone or corticosterone predicted dewlap size and/or bite-force capacity, as dewlap size is known to be a reliable predictor of bite-force capacity in territorial males. We also examined whether these relationships were consistent between previously described body size classes ("lightweights" and "heavyweights"). Heavyweights had 50% higher testosterone concentrations than lightweights during the breeding season, suggesting a mechanism for the disproportionately larger heads and dewlaps and higher bite-forces of heavyweights. Plasma testosterone concentrations were positively correlated with dewlap size and bite-force performance in lightweights (but not heavyweights) but only because of mutual intercorrelation of all three variables with body size. We suggest two possibilities for the relationship between testosterone levels and body size: (1) testosterone promotes growth in this species or (2) smaller sexually mature males are unable to compete with larger males such that the benefits of elevated testosterone do not outweigh the costs. Corticosterone levels did not differ between the male morphs, and lightweights, but not heavyweights, showed an inverse relationship between testosterone levels and corticosterone levels. Our results suggest that testosterone is important for traits related to dominance in adult male green anoles and may influence the ability to compete with rivals via fighting ability or through the use of signals.     

The incredible shrinking dewlap: signal size,skin elasticity,and mechanical design in the green anole lizard (Anolis carolinensis)

The expression of male secondary sexual traits can be dynamic, changing size, shape, color, or structure over the course of different seasons. However, the factors underlying such changes are poorly understood. In male Anolis carolinensis lizards, a morphological secondary sexual signal called the dewlap changes size seasonally within individuals. Here, we test the hypothesis that seasonal changes in male dewlap size are driven by increased use and extension of the dewlap in spring and summer, when males are breeding, relative to the winter and fall. We captured male green anole lizards prior to the onset of breeding and constrained the dewlap in half of them such that it could not be extended. We then measured dewlap area in the spring, summer, and winter, and dewlap skin and belly skin elasticity in summer and winter. Dewlaps in unconstrained males increase in area from spring to summer and then shrink in the winter, whereas the dewlaps of constrained males consistently shrink from spring to winter. Dewlap skin is significantly more elastic than belly skin, and skin overall is more elastic in the summer relative to winter. These results show that seasonal changes in dewlap size are a function of skin elasticity and display frequency, and suggest that the mechanical properties of signaling structures can have important implications for signal evolution and design.     

Are morphology–performance relationships invariant across different seasons? A test with the green anole lizard (Anolis carolinensis)

A key assumption in ecomorphological studies is that morphology–function relationships are invariant due to underlying biomechanical principles. We tested the hypothesis that morphology–performance relationships are invariant across different seasons by examining how a key performance trait, bite force, and two aspects of morphology (head shape and dewlap size) changed seasonally in the field and in the laboratory in the green anole lizard Anolis carolinensis . We found that not only did bite force change seasonally (up to 80% within the same individual), but relationships between morphology and bite force are highly plastic. Of the three traits examined (bite force, head shape, and dewlap area), only head shape did not change seasonally. We noted opposing trends for how bite force and dewlap area changed seasonally; whereas dewlap areas were large in the spring, and small in the winter, bite forces were low in the spring and high in the winter. This pattern occurred because of a tradeoff at the individual level: individuals in the spring with large dewlaps and high bite forces diminish their dewlaps (but not bite force), whereas individuals with small dewlaps and low bite forces in the spring increase their bite forces (but not dewlap size). We also show that this trend was apparent both in the field (comparing different individuals) and the laboratory (comparing the same set of individuals under standardized conditions). Finally, seasonal changes were not consistent among individuals for either bite force or dewlap area, as individuals changed seasonally in proportion to their initial state. These findings cast doubt on the widely held view of invariant morphology–performance relationships, and offer a cautionary note for eco-morphological studies.     

Hybridization and rapid differentiation after secondary contact between the native green anole (Anolis carolinensis) and the introduced green anole (Anolis porcatus)

In allopatric species, reproductive isolation evolves through the accumulation of genetic incompatibilities. The degree of divergence required for complete reproductive isolation is highly variable across taxa, which makes the outcome of secondary contact between allopatric species unpredictable. Since before the Pliocene, two species of Anolis lizards, Anolis carolinensis and Anolis porcatus, have been allopatric, yet this period of independent evolution has not led to substantial species‐specific morphological differentiation, and therefore, they might not be reproductively isolated. In this study, we determined the genetic consequences of localized, secondary contact between the native green anole, A. carolinensis, and the introduced Cuban green anole, A. porcatus, in South Miami. Using 18 microsatellite markers, we found that the South Miami population formed a genetic cluster distinct from both parental species. Mitochondrial DNA revealed maternal A. porcatus ancestry for 35% of the individuals sampled from this population, indicating a high degree of cytonuclear discordance. Thus, hybridization with A. porcatus, not just population structure within A. carolinensis, may be responsible for the genetic distinctiveness of this population. Using tree‐based maximum‐likelihood analysis, we found support for a more recent, secondary introduction of A. porcatus to Florida. Evidence that ~33% of the nuclear DNA resulted from a secondary introduction supports the hybrid origin of the green anole population in South Miami. We used multiple lines of evidence and multiple genetic markers to reconstruct otherwise cryptic patterns of species introduction and hybridization. Genetic evidence for a lack of reproductive isolation, as well as morphological similarities between the two species, supports revising the taxonomy of A. carolinensis to include A. porcatus from western Cuba. Future studies should target the current geographic extent of introgression originating from the past injection of genetic material from Cuban green anoles and determine the consequences for the evolutionary trajectory of green anole populations in southern Florida.     

Performance capacity, fighting tactics and the evolution of life-stage male morphs in the green anole lizard (Anolis carolinensis)

The evolution of alternative male phenotypes is probably driven by male-male competition for access to reproductive females, but few studies have examined whether whole-organism performance capacities differ between male morphs, and if so whether any such differences affect fighting ability. We show how ontogenetic changes in performance and morphology have given rise to two distinct life-stage male morphs exhibiting different fighting tactics within the green anole lizard (Anolis carolinensis). Field studies show a bimodal distribution of adult males within a single population: larger 'heavyweight' males have relatively large heads and high bite forces for their size, whereas smaller 'lightweight' males have smaller heads and lower bite forces. In staged fights between size-matched heavyweight males, males with greater biting ability won more frequently, whereas in lightweight fights, males with greater jumping velocity and acceleration won more often. Because growth in reptiles is indeterminate, and the anole males examined are sexually mature, we propose that the heavyweight morph arose through selection against males with small heads and poor bite forces at the lightweight-heavyweight size transition. Our findings imply that one may not be able to predict male fighting success (and hence potential mating success) by examining aspects of male 'quality' at only one life stage.     

A performance-based cost to honest signalling in male green anole lizards (Anolis carolinensis)

Sexual signals are considered costly to produce and maintain under the handicap paradigm, and the reliability of signals is in turn thought to be maintained by these costs. Although previous studies have investigated the costly nature of signal production, few have considered whether honesty might be maintained not by the costliness of the signal itself, but by the costs involved in producing the signalled trait. If such a trait is itself costly to produce, then the burden of energetic investment may fall disproportionately on that trait, in addition to any costs of signal maintenance that may also be operating. Under limited resource conditions, these costs may therefore be great enough to disrupt an otherwise reliable signal-to-trait relationship. We present experimental evidence showing that dietary restriction decouples the otherwise honest relationship between a signal (dewlap size) and a whole-organism performance trait (bite force) in young adult male Anolis carolinensis lizards. Specifically, while investment in dewlap size is sustained under low-resource condition relative to the high-resource treatment, investment in bite force is substantially lower. Disruption of the otherwise honest dewlap size to bite force relationship is therefore driven by costs associated with the expression of performance rather than the costs of signal production in A. carolinensis.     

The green anole (Anolis carolinensis): a reptilian model for laboratory studies of reproductive morphology and behavior

The green anol (Anolis carolinensis) is an excellent reptilian model for studying reproductive behavior and the neural and muscular morphology that supports it. This lizard has been the subject of behavioral and ecological study for more than 100 yr, and a rich literature exists on its natural history. Both courtship and copulatory behaviors reveal sex and seasonal differences, which allow for the study of mechanisms regulation naturally occurring variation in performance at multiple levels within a single animal model. Green anoles are readily obtained due to their abundance in the wild; once in the laboratory, they are easily maintained, bred, and reared. Background on the natural history and husbandry of this lizard is provided, and the authors' research program on the regulation of reproductive anatomy and behavior is reviewed, Discussion includes the similarities and differences in the mechanisms mediating both structure and function compared with more traditional animal models. This type of comparative research will make it possible to identify the fundamental principles governing reproductive biology, thus advancing both basic and applied knowledge.     

Genetic variation in the green anole lizard (Anolis carolinensis) reveals island refugia and a fragmented Florida during the quaternary

The green anole lizard (Anolis carolinensis) is a model organism for behavior and genomics that is native to the southeastern United States. It is currently thought that the ancestors of modern green anoles dispersed to peninsular Florida from Cuba. However, the climatic changes and geological features responsible for the early diversification of A. carolinensis in North America have remained largely unexplored. This is because previous studies (1) differ in their estimates of the divergence times of populations, (2) are based on a single genetic locus or (3) did not test specific hypotheses regarding the geologic and topographic history of Florida. Here we provide a multi-locus study of green anole genetic diversity and find that the Florida peninsula contains a larger number of genetically distinct populations that are more diverse than those on the continental mainland. As a test of the island refugia hypothesis in Pleistocene Florida, we use a coalescent approach to estimate the divergence times of modern green anole lineages. We find that all demographic events occurred during or after the Upper Pliocene and suggest that green anole diversification was driven by population divergence on interglacial island refugia in Florida during the Lower Pleistocene, while the region was often separated from continental North America. When Florida reconnected to the mainland, two separate dispersal events led to the expansion of green anole populations across the Atlantic Seaboard and Gulf Coastal Plain.     

Evidence of divergent growth rates among populations of the lizard Anolis carolinensis based on experimental manipulations of egg size

Geographic variation in body size is of special interest because it affects nearly all aspects of an organism’s life. I examined whether differences in body size among four populations of the green anole lizard, Anolis carolinensis, were attributable to maternal investment in egg size and/or growth rates of embryos and juveniles. Larger body size and larger egg size relative to female size in the northern part of the range have been documented in this species, and suggested to be adaptive responses to more extreme winters. The current study confirmed the trends in adult size and egg size in the north, but rejected the trend of larger egg size relative to body size in the south. To control for differences in maternal investment in egg size among populations, I performed yolk removals on eggs from two northern populations to produce comparably sized eggs relative to one southern population. This manipulation was designed to minimize the confounding effect of maternal investment in yolk, the primary energy reserves for eggs, so that intrinsic differences in embryonic growth due to metabolism could be investigated. I found that differences in juvenile and, potentially, embryonic growth rates existed among populations of A. carolinensis, both due to and independent of differences in egg size. Juveniles from the northernmost population were bigger not only due to larger egg size, but also due to faster juvenile growth and possibly differences in developmental stage of oviposition or conversion of egg mass to hatchling mass. Larger body size may hold a number of advantages in northern populations of this species, including starvation resistance through winters and better competitive access to food resources and warmer microhabitats.     

The maternal energetic environment affects both egg and offspring phenotypes in green anole lizards (Anolis carolinensis)

Animals exist in dynamic environments that may affect both their own fitness and that of their offspring. Maternal effects might allow mothers to prepare their offspring for the environment in which they will be born via several mechanisms, not all of which are well understood. Resource scarcity and forced resource allocation are two scenarios that could affect maternal investment by altering the amount and type of resources available for investment in offspring, albeit in potentially different ways. We tested the hypothesis that maternal dietary restriction and sprint training have different consequences for the offspring phenotype in an oviparous lizard (Anolis carolinensis). To do this, we collected and reared eggs from adult diet-manipulated females (low-diet [LD] or high-diet [HD]) and sprint-trained females (sprint trained [ST] or untrained [UT]) and measured both egg characteristics and hatchling morphology. ST and LD mothers laid both the fewest and heaviest eggs, and ST, UT, and LD eggs also had significantly longer incubation periods than the HD group. Hatchlings from the diet experiment (LD and HD offspring) were the heaviest overall. Furthermore, both body mass of the mother at oviposition and change in maternal body mass over the course of the experiment had significant and sometimes different effects on egg and offspring phenotypes, highlighting the importance of maternal energetic state to the allocation of maternal resources.     

Assessment of the mass,length, center of mass,and principal moment of inertia of body segments in adult males of the brown anole (Anolis sagrei) and green,or carolina,anole (Anolis carolinensis)

This study provides a morphometric data set of body segments that are biomechanically relevant for locomotion in two ecomorphs of adult male anoles, namely, the trunk‐ground Anolis sagrei and the trunk‐crown Anolis carolinensis. For each species, 10 segments were characterized, and for each segment, length, mass, location of the center of mass, and radius of gyration were measured or calculated, respectively. The radii of gyration were computed from the moments of inertia by using the double swing pendulum method. The trunk‐ground A. sagrei has relatively longer and stockier hindlimbs and forelimbs with smaller body than A. carolinensis. These differences between the two ecomorphs demonstrated a clear relationship between morphology and performance, particularly in the context of predator avoidance behavior, such as running or jumping in A. sagrei and crypsis in A. carolinensis. Our results provide new perspectives on the mechanism of adaptive radiation as the limbs of the two species appear to scale via linear factors and, therefore, may also provide explanations for the mechanism of evolutionary changes of structures within an ecological context. J. Morphol., 2012. © 2012 Wiley Periodicals, Inc.     

Evolutionary relationships between morphology, performance and habitat openness in the lizard genus Niveoscincus (Scincidae: Lygosominae)

Correlations between an animal's morphology and ecological parameters such as habitat characteristics emphasize the intimate link between phenotype and the environment, but are often difficult to interpret because the functional consequences of morphological variation are frequently unknown. We provide one of the few studies relating limb morphology, functional capabilities, and habitat in reptiles. We tested the hypothesis that species occupying open microhabitats would possess relatively longer limbs and faster sprint speeds than those occurring in more closed microhabitats. A number of morphological characteristics relevant to locomotion were quantified, including the length of the bones of the fore- and hindlimbs and body size. A phylogenetic analysis was then used to examine the evolutionary relationships between morphology, locomotor performance and microhabitat openness in seven species of Niveoscincus and one species of the closely related genus Pseudemoia. A significant evolutionary relationship was established between sprinting ability, morphology, and the openness of the microhabitat occupied by a species. The phylogenetic analysis demonstrated an evolutionary trend in Niveoscincus of species occupying open microhabitats (e.g. N. greeni, N ocellatus) being large with long limbs and high sprinting ability, while those occupying closed microhabitats (e.g. N coventryi, P. entrecasteauxii) art smaller with short limbs and much slower maximum sprint speeds.     

Independent introductions and sequential founder events shape genetic differentiation and diversity of the invasive green anole (Anolis carolinensis) on Pacific Islands

Aim

Natural range expansions and human‐mediated colonizations usually involve a small number of individuals that establish new populations in novel habitats. In both cases, founders carry only a fraction of the total genetic variation of the source populations. Here, we used native and non‐native populations of the green anole, Anolis carolinensis, to compare the current distribution of genetic variation in populations shaped by natural range expansion and human‐mediated colonization.

Location

North America, Hawaiian Islands, Western Pacific Islands.

Methods

We analysed 401 mtDNA haplotypes to infer the colonization history of A. carolinensis on nine islands in the Pacific Ocean. We then genotyped 576 individuals at seven microsatellite loci to assess the levels of genetic diversity and population genetic differentiation for both the native and non‐native ranges.

Results

Our findings support two separate introductions to the Hawaiian Islands and several western Pacific islands, with subsequent colonizations within each region following a stepping‐stone model. Genetic diversity at neutral markers was significantly lower in the non‐native range because of founder effects, which also contributed to the increased population genetic differentiation among the non‐native regions. In contrast, a steady reduction in genetic diversity with increasing distance from the ancestral population was observed in the native range following range expansion.

Main conclusions

Range expansions cause serial founder events that are the spatial analogue of genetic drift, producing a pattern of isolation‐by‐distance in the native range of the species. In human‐mediated colonizations, after an initial loss of genetic diversity, founder effects appear to persist, resulting in overall high genetic differentiation among non‐native regions but an absence of isolation‐by‐distance. Contrasting the processes influencing the amount and structuring of genetic variability during natural range expansion and human‐mediated biological invasions can shed new light on the fate of natural populations exposed to novel and changing environments.

     

Geographical variation in morphology and its environmental correlates in a widespread North American lizard,Anolis carolinensis (Squamata: Dactyloidae)

The green anole, Anolis carolinensis, has long been an important model organism for studies of physiology and behaviour, and recently became the first reptile to have its genome sequenced. With a large and environmentally heterogeneous distribution, especially in relation to well‐studied Antillean relatives, A. carolinensis is also emerging as an important organism for novel studies of geographical differentiation and adaptation. In the present study, we quantify the degree of morphological variation in this species and test for environmental correlates of this variation. We also examine adherence to Bergmann's and Allen's rule, two eco‐geographical principles that have been well studied over large species ranges. We sampled from 14 populations across the distribution of the species in North America and measured 28 distinct morphological traits. We also collected a suite of environmental variables for each site, including those related to temperature, precipitation, and vegetation. Ultimately, we found a large degree of geographical variation in morphology, with head traits contributing the most to differences among populations. Morphological variation was correlated with variation in temperature, precipitation, and latitude across sites. We found no support for reverse Bergmann's rule typical of squamates, although we did find a trend of reverse Allen's rule. Ultimately, the present study provides a novel look at A. carolinensis and establishes it as a strong candidate for further studies of variation and adaptation over a large range.