Anolis Sagrei Research Articles

Observing character displacement from process to pattern in a novel vertebrate community.

Ecological character displacement, whereby shifts in resource use in the presence of competing species leads to adaptive evolutionary divergence, is widely considered an important process in community assembly and adaptive radiation. However, most evidence for character displacement has been inferred from macro-scale geographic or phylogenetic patterns; direct tests of the underlying hypothesis of divergent natural selection driving character displacement in the wild are rare. Here, we document character displacement between two ecologically similar lizards (Anolis sagrei and A. cristatellus) experiencing novel contact. We identify directional selection during the incipient stages of sympatry in a new community that corresponds to repeated trait divergence across multiple established sympatric communities. By identifying the role of natural selection as character displacement unfolds, we connect how natural selection operating at short timescales may drive broader patterns of trait distributions at larger spatial and temporal scales.

Developmental reaction norms vary among families of lizards in response to multivariate nest environments

Developmental plasticity is the capacity of a single genotype to express multiple phenotypes in response to different early‐life environments. Such responses are defined by reaction norms, which may vary among individuals or populations. Variation in developmental reaction norms allows natural selection to operate on plasticity and is rarely examined in vertebrates. We quantified variation in embryonic developmental plasticity within and between populations using the brown anole lizard. We captured lizards from two islands in the Matanzas River (Florida, USA) and incubated their eggs under one of two multivariate treatments that mimicked the temperature, moisture and substrates of nest sites in either a shaded or open habitat. We measured hatchling morphology, performance, and physiology to quantify variation in family‐level reaction norms. We observed evidence of family‐level variation in reaction norms for morphology but not for performance or physiology, indicating an opportunity for natural selection to shape plasticity in hatchling body size. Overall, the results indicate that multiple abiotic conditions in natural nests combine to increase or reduce phenotypic variation, and that family‐level variation in reaction norms provides a potential for natural selection to shape plasticity.

Meta-Analysis Reveals Behavioral Plasticity, Not Agonistic Behavior, Facilitates Invasion of Brown Anoles (Anolis sagrei) and Replacement of Green Anoles (Anolis carolinensis)

In a meta-analysis, we examined the behavioral portfolio of invasive brown anoles (Anolis sagrei) and native green anoles (Anolis carolinensis) in urban and non-urban environments. We hypothesized that invasive anoles would display more agonistic and bold signals (head bobbing, dewlap extensions, and pushups) than their native-range counterparts and their native competitors. We found that in urban settings, anoles of both species signaled more with dewlap extensions than with head bobs. Brown anoles displayed significantly more in non-urban habitats and their native range compared to urban habitats and invasive ranges. The outcome of our analysis suggests that brown anoles have plastic behavioral portfolios, whereas green anoles have relatively balanced preferences for head bobbing, irrespective of the habitat in which the populations were collected. We attribute the success of the brown anole invasion to the flexible strategy in the face of higher mate competition, higher predation risks, and less resource competition in both urban and invasive ranges. Lastly, we observed publication biases. More studies were conducted with urban and invasive brown anoles and specifically in manipulative mesocosm experimental settings—transplanting populations from native field settings. We show this altered the display rates across all studied signals.

Within the optimal thermal range, temperature fluctuations with similar means have little effect on offspring phenotypes: A comparison of two approaches that simulate natural nest conditions

Temperature influences nearly every aspect of organismal function. Because aspects of global change such as urbanization and climate change influence temperature, researchers must consider how altering thermal regimes will impact biodiversity across the planet. To do so, they often measure temperature in natural and/or human-modified habitats, replicate those temperatures in laboratory experiments to understand organismal responses, and make predictions under models of future change. Consequently, accurately representing temperature in the laboratory is an important concern, yet few studies have assessed the consequences of simulating thermal conditions in different ways. We used nest temperatures for two urban-dwelling, invasive lizards (Anolis sagrei and A. cristatellus) to create two egg incubation treatments in the laboratory. Like most studies of thermal developmental plasticity, we created daily repeating thermal fluctuations; however, we used different methods to create temperature treatments that differed in the magnitude and breadth of thermal cycles, and then evaluated the effects of these different approaches on embryo development and hatchling phenotypes. Additionally, we measured embryo heart rate, a proxy for metabolism, across temperature to understand the immediate effects of treatments. We found that treatments had minimal effect on phenotypes likely because temperatures were within the optimal thermal range for each species and were similar in mean temperature. We conclude that slight differences in thermal treatments may be unimportant so long as temperatures are within a range appropriate for development, and we make several recommendations for future studies of developmental plasticity.

Limited Morphological Differences of Brown Anoles (Anolis sagrei) between Their Native Cuban and Invasive Florida Range

Limited Morphological Differences of Brown Anoles (Anolis sagrei) between Their Native Cuban and Invasive Florida Range

Anolis sagrei – A Novel Reptile Model for Studying the Role of the Macular Carotenoids in the Retina

Anolis sagrei – A Novel Reptile Model for Studying the Role of the Macular Carotenoids in the Retina

Structural analysis of the female reptile reproductive system by micro-computed tomography and optical coherence tomography†.

Volumetric data provide unprecedented structural insight to the reproductive tract and add vital anatomical context to the relationships between organs. The morphology of the female reproductive tract in non-avian reptiles varies between species, corresponding to a broad range of reproductive modes and providing valuable insight to comparative investigations of reproductive anatomy. However, reproductive studies in reptilian models, such as the brown anole studied here, have historically relied on histological methods to understand the anatomy. While these methods are highly effective for characterizing the cell types present in each organ, histological methods lose the 3D relationships between images and leave the architecture of the organ system poorly understood. We present the first comprehensive volumetric analyses of the female brown anole reproductive tract using two non-invasive, non-destructive imaging modalities: micro-computed tomography (microCT) and optical coherence tomography (OCT). Both are specialized imaging technologies that facilitate high-throughput imaging and preserve three-dimensional information. This study represents the first time that microCT has been used to study all reproductive organs in this species and the very first time that OCT has been applied to this species. We show how the non-destructive volumetric imaging provided by each modality reveals anatomical context including orientation and relationships between reproductive organs of the anole lizard. In addition to broad patterns of morphology, both imaging modalities provide the high resolution necessary to capture details and key anatomical features of each organ. We demonstrate that classic histological features can be appreciated within whole-organ architecture in volumetric imaging using microCT and OCT, providing the complementary information necessary to understand the relationships between tissues and organs in the reproductive system. This side-by-side imaging analysis using microCT and OCT allows us to evaluate the specific advantages and limitations of these two methods for the female reptile reproductive system.

On the role of TFEC in reptilian coloration.

Reptilian species, particularly snakes and lizards, are emerging models of animal coloration. Here, I focus on the role of the TFEC transcription factor in snake and lizard coloration based on a study on wild-type and piebald ball pythons. Genomic mapping previously identified a TFEC mutation linked to the piebald ball python phenotype. The association of TFEC with skin coloration was further supported by gene-editing experiments in the brown anole lizard. However, novel histological analyses presented here reveal discrepancies between the ball python and the anole TFEC mutants phenotype, cautioning against broad generalizations. Indeed, both wild-type and piebald ball pythons completely lack iridophores, whereas the TFEC anole lizard mutants lose their iridophores compared to the wild-type anole. Based on these findings, I discuss the potential role of the MiT/TFE family in skin pigmentation across vertebrate lineages and advocate the need for developmental analyses and additional gene-editing experiments to explore the reptilian coloration diversity.

First record of Anolis sagrei Dumeril & Bibron, 1837 (Squamata, Anolidae) in Sonora, northwestern Mexico

Anolis sagrei is a lizard that naturally occurs on various islands of the Caribbean and in Central America. However, it has also been widely introduced in different countries around the world. In Mexico, it is present in seven states with tropical climate Here, we present the first record of A. sagrei from the Mexican state of Sonora.

Updated distribution of the brown anole in continental Ecuador: a case of urban spaces favoring the establishment of an opportunistic exotic species

Updated distribution of the brown anole in continental Ecuador: a case of urban spaces favoring the establishment of an opportunistic exotic species

Behavioral estimates of mating success corroborate genetic evidence for pre-copulatory selection

Abstract In promiscuous species, fitness estimates obtained from genetic parentage may often reflect both pre- and post-copulatory components of sexual selection. Directly observing copulations can help isolate the role of pre-copulatory selection, but such behavioral data are difficult to obtain in the wild and may also overlook post-copulatory factors that alter the relationship between mating success and reproductive success. To overcome these limitations, we combined genetic parentage analysis with behavioral estimates of size-specific mating in a wild population of brown anole lizards (Anolis sagrei). Males of this species are twice as large as females and multiple mating among females is common, suggesting the scope for both pre- and post-copulatory processes to shape sexual selection on male body size. Our genetic estimates of reproductive success revealed strong positive directional selection for male size, which was also strongly associated with the number of mates inferred from parentage. In contrast, a male’s size was not associated with the fecundity of his mates or his competitive fertilization success. By simultaneously tracking copulations in the wild via the transfer of colored powder to females by males from different size quartiles, we independently confirmed that large males were more likely to mate than small males. We conclude that body size is primarily under pre-copulatory sexual selection in brown anoles, and that post-copulatory processes do not substantially alter the strength of this selection. Our study also illustrates the utility of combining both behavioral and genetic methods to estimate mating success to disentangle pre- and post-copulatory processes in promiscuous species.

Predator-driven behavioural shifts in a common lizard shape resource-flow from marine to terrestrial ecosystems.

Foraging decisions shape the structure of food webs. Therefore, a behavioural shift in a single species can potentially modify resource-flow dynamics of entire ecosystems. To examine this, we conducted a field experiment to assess foraging niche dynamics of semi-arboreal brown anole lizards in the presence/absence of predatory ground-dwelling curly-tailed lizards in a replicated set of island ecosystems. One year after experimental translocation, brown anoles exposed to these predators had drastically increased perch height and reduced consumption of marine-derived food resources. This foraging niche shift altered marine-to-terrestrial resource-flow dynamics and persisted in the diets of the first-generation offspring. Furthermore, female lizards that displayed more risk-taking behaviours consumed more marine prey on islands with predators present. Our results show how predator-driven rapid behavioural shifts can alter food-web connectivity between oceanic and terrestrial ecosystems and underscore the importance of studying behaviour-mediated niche shifts to understand ecosystem functioning in rapidly changing environments.

A high-quality genome for the slender anole (Anolis apletophallus): an emerging model for field studies of tropical ecology and evolution.

The slender anole, Anolis apletophallus, is a small arboreal lizard of the rainforest understory of central and eastern Panama. This species has been the subject of numerous ecological and evolutionary studies over the past 60 years as a result of attributes that make it especially amenable to field and laboratory science. Slender anoles are highly abundant, short-lived (nearly 100% annual turnover), easy to manipulate in both the lab and field, and are ubiquitous in the forests surrounding the Smithsonian Tropical Research Institute in Panama, where researchers have access to high-quality laboratory facilities. Here, we present a high-quality genome for the slender anole, which is an important new resource for studying this model species. We assembled and annotated the slender anole genome by combining 3 technologies: Oxford Nanopore, 10× Genomics Linked-Reads, and Dovetail Omni-C. We compared this genome with the recently published brown anole (Anolis sagrei) and the canonical green anole (Anolis carolinensis) genomes. Our genome is the first assembled for an Anolis lizard from mainland Central or South America, the regions that host the majority of diversity in the genus. This new reference genome is one of the most complete genomes of any anole assembled to date and should facilitate deeper studies of slender anole evolution, as well as broader scale comparative genomic studies of both mainland and island species. In turn, such studies will further our understanding of the well-known adaptive radiation of Anolis lizards.

Stronger evidence for genetic ancestry than environmental conditions in shaping the evolution of a complex signalling trait during biological invasion.

Introductions of invasive species to new environments often result in rapid rates of trait evolution. While in some cases these evolutionary transitions are adaptive and driven by natural selection, they can also result from patterns of genetic and phenotypic variation associated with the invasion history. Here, we examined the brown anole (Anolis sagrei), a widespread invasive lizard for which genetic data have helped trace the sources of non-native populations. We focused on the dewlap, a complex signalling trait known to be subject to multiple selective pressures. We measured dewlap reflectance, pattern and size in 30 non-native populations across the southeastern United States. As well, we quantified environmental variables known to influence dewlap signal effectiveness, such as canopy openness. Further, we used genome-wide data to estimate genetic ancestry, perform association mapping and test for signatures of selection. We found that among-population variation in dewlap characteristics was best explained by genetic ancestry. This result was supported by genome-wide association mapping, which identified several ancestry-specific loci associated with dewlap traits. Despite the strong imprint of this aspect of the invasion history on dewlap variation, we also detected significant relationships between dewlap traits and local environmental conditions. However, we found limited evidence that dewlap-associated genetic variants have been subject to selection. Our study emphasizes the importance of genetic ancestry and admixture in shaping phenotypes during biological invasion, while leaving the role of selection unresolved, likely due to the polygenic genetic architecture of dewlaps and selection acting on many genes of small effect.

Maturation and refinement of the maculae and foveae in the Anolis sagrei lizard

The fovea is a pit in the center of the macula, which is a region of the retina with a high concentration of photoreceptor cells, which accounts for a large degree of visual acuity in primates. The maturation of this primate visual acuity area is characterized by the shallowing and widening of the foveal pit, a decrease in the diameter of the rod-free zone, and an increase in photoreceptor cells packing after birth. Maturation occurs concurrently with progressing age, increasing eye size, and retinal length/area. These observations have led to the hypothesis that the maturation of the fovea might be a function of mechanical variables that remodel the retina. However, this has never been explored outside of primates. Here, we take advantage of the Anolis sagrei lizard, which has a bifoveated retina, to study maturation of the fovea and macula. Eyes were collected from male and female lizards–hatchling, 2-month, 4-month, 6-month, and adult. We found that Anolis maculae undergo a maturation process somewhat different than what has been observed in primates. Anole macular diameters actually increase in size and undergo minimal photoreceptor cell packing, possessing a near complete complement of these cells at the time of hatching. As the anole eye expands, foveal centers experience little change in overall retina cell density with most cell redistribution occurring at macular borders and peripheral retina areas. Gene editing technology has recently been developed in lizards; this study provides a baseline of normal retina maturation for future genetic manipulation studies in anoles.

Anatomy of the female reproductive tract organs of the brown anole (Anolis sagrei).

Female reproduction in squamate reptiles (lizards and snakes) is highly diverse and mode of reproduction, clutch size, and reproductive tract morphology all vary widely across this group of ~11,000 species. Recently, CRISPR genome editing techniques that require manipulation of the female reproductive anatomy have been developed in this group, making a more complete understanding of this anatomy essential. We describe the adult female reproductive anatomy of the model reptile the brown anole (Anolis sagrei). We show that the brown anole female reproductive tract has three distinct anterior-to-posterior regions, the infundibulum, the glandular uterus, and the nonglandular uterus. The infundibulum has a highly ciliated epithelial lip, a region where the epithelium is inverted so that cilia are present on the inside and outside of the tube. The glandular uterus has epithelial ducts that are patent with a lumen as well as acinar structures with a lumen. The nonglandular uterus has a heterogeneous morphology from anterior to posterior, with a highly folded, ciliated epithelium transitioning to a stratified squamous epithelium. This transition is accompanied by a loss of keratin-8 expression and together, these changes are similar to the morphological and gene expression changes that occur in the mammalian cervix. We recommend that description of the nonglandular uterus include the regional sub-specification of a "cervix" and "vagina" as this terminology change more accurately describes the morphology. Our data extend histological studies of reproductive organ morphology in reptiles and expand our understanding of the variation in reproductive system anatomy across squamates and vertebrates.

Bite or flight? Behavioral interactions between bark anoles and brown anoles in their nonnative range

AbstractBoth intra‐ and interspecific interactions play crucial roles in defining the structure of ecological communities. However, the specific behavioral processes underlying this structuring are often unclear and must be inferred from contemporary interactions. Rapid spread of nonnative species has resulted in increasingly homogenized communities, and this homogenization provides an excellent opportunity to study the behavioral processes that lead to stable communities of introduced species in novel habitats. Here, we compared the behavior of brown anoles (Anolis sagrei) and bark anoles (A. distichus) when faced with an incursion by an unknown brown anole to examine the intra‐ and interspecific interactions underlying the structuring of novel communities in South Florida, USA. We found that brown anoles were consistently more aggressive toward intruders than bark anoles, and this pattern was accentuated when they encountered intruders of the same sex. Conversely, bark anoles were likely to flee when they encountered intruder brown anoles. We also found that brown anoles were likely to attack intruders regardless of whether they engaged in aggressive behavioral displays while bark anoles were likely to flee regardless of whether the intruder engaged in behavioral displays. Our findings suggest that behavioral interactions could play a significant role in structuring the novel Anolis communities in South Florida and demonstrate the importance of aggressive interactions both within and between species.

Experimentally simulating the evolution-to-ecology connection: Divergent predator morphologies alter natural food webs

The idea that changing environmental conditions drive adaptive evolution is a pillar of evolutionary ecology. But, the opposite-that adaptive evolution alters ecological processes-has received far less attention yet is critical for eco-evolutionary dynamics. We assessed the ecological impact of divergent values in a key adaptive trait using 16 populations of the brown anole lizard (Anolis sagrei). Mirroring natural variation, we established islands with short- or long-limbed lizards at both low and high densities. We then monitored changes in lower trophic levels, finding that on islands with a high density of short-limbed lizards, web-spider densities decreased and plants grew more via an indirect positive effect, likely through an herbivore-mediated trophic cascade. Our experiment provides strong support for evolution-to-ecology connections in nature, likely closing an otherwise well-characterized eco-evolutionary feedback loop.

Multisystemic Enterococcosis in Brown Anoles (Anolis sagrei) from Florida, USA.

Beginning in July 2019, numerous free-ranging brown anoles (Anolis sagrei), an invasive lizard species in Florida, USA, were reported with large, soft, subcutaneous masses and disfiguring facial swellings. Postmortem evaluations of six affected animals, including cytology, histology, and electron microscopy, identified the presence of myriad chain-forming coccoid bacteria surrounded by a prominent clear capsule and abundant lightly basophilic matrix material with minimal associated granulomatous inflammation and effacement of normal tissue. Standard PCR and sequencing of the lesions revealed 100% nucleotide identity to Enterococcus lacertideformus. This bacterium was first observed in 2014 as the cause of a severe, multisystemic infection in several species of lizards (geckos and skinks) on Christmas Island, an Australian external territory in the Indian Ocean. Previously, analysis of E. lacertideformus had been hindered by an inability to grow the bacterium in standard culture conditions. We successfully cultured the organism on primary anole kidney cells. Given the growing recognition of host species diversity and geographic distribution noted for this organism, there is potential concern for spread to native North American lizards, especially the green anole (Anolis carolinensis), whose population numbers have apparently decreased due to introduced brown anoles.

Amphibians and reptiles of Isla Santay (Durán, Ecuador)

Amphibian and reptile diversity from Isla Santay (Durán, Ecuador) has been underestimated due to the lack of monitoring throughout the island. Historically, this island has also been affected by anthropic landscape changes which limit the occurrence of certain species and favors the dispersion of opportunistic or more tolerant species. Such species dynamics tend to be more evident on islands, since their isolation limits species’ mobility. We present an updated checklist of the herpetofauna of Isla Santay Durán, Ecuador, and report for the first time the occurrence of two introduced species, Anolis sagrei Duméril & Bibron, 1837, Brown Anole, and Hemydactylus frenatus Duméril & Bibron, 1836.