The Evolution of Diet and Morphology in Insular Lizards: Insights from a Replicated Island Introduction Experiment.

Resource-limited environments may drive the rapid evolution of phenotypic traits and ecological preferences optimizing the exploitation of resources. Very small islands are often characterized by reduced food availability, seasonal fluctuations in resources and strong unpredictability. These features may drive the evolution of phenotypic traits such as high bite forces, allowing animals to exploit a wider variety of the available resources. They may also lead to more generalist dietary patterns in response to food scarcity. However, the lack of predators and competitors on such small islands often also leads to high densities and the evolution of strong sexual dimorphism, which may also drive the evolution of bite force. Here, we take advantage of a unique replicated introduction experiment to test whether lizards introduced into very small islands alter their feeding ecology and use different resources, resulting in the evolution of a large body size, large head size and large bite forces. Our results show that three years after their introduction, the island lizards were larger and had greater bite forces and more pronounced sexual dimorphism. However, the diets were only marginally different between animals from the source population on a very large nearby island and those on the islets. Moreover, distinct differences in diet between animals on the different islets were observed, suggesting that the local environment is a strong driver of resource use. Overall, lizards with absolutely and relatively (adjusted for body size) large bite forces did eat larger and harder prey. Taken together, our data suggest that intraspecific competition is an important driver of the rapid evolution of bite force, which may allow these lizards to exploit the scarce and fluctuating resources on the islets. Whether or not lizards will evolve to include other types of food such as plants in their diet, facilitated by their large bite forces, remains to be explored in future studies.

Can extreme climatic events induce shifts in adaptive potential? A conceptual framework and empirical test with Anolis lizards.

Multivariate adaptation to climatic shifts may be limited by trait integration that causes genetic variation to be low in the direction of selection. However, strong episodes of selection induced by extreme climatic pressures may facilitate future population-wide responses if selection reduces trait integration and increases adaptive potential (i.e., evolvability). We explain this counter-intuitive framework for extreme climatic events in which directional selection leads to increased evolvability and exemplify its use in a case study. We tested this hypothesis in two populations of the lizard Anolis scriptus that experienced hurricane-induced selection on limb traits. We surveyed populations immediately before and after the hurricane as well as the offspring of post-hurricane survivors, allowing us to estimate both selection and response to selection on key functional traits: forelimb length, hindlimb length, and toepad area. The direct selection was parallel in both islands and strong in several limb traits. Even though overall limb integration did not change after the hurricane, both populations showed a non-significant tendency toward increased evolvability after the hurricane despite the direction of selection not being aligned with the axis of most variance (i.e., body size). The population with comparably lower between-limb integration showed a less constrained response to selection. Hurricane-induced selection, not aligned with the pattern of high trait correlations, likely conflicts with selection occurring during normal ecological conditions that favours functional coordination between limb traits, and would likely need to be very strong and more persistent to elicit a greater change in trait integration and evolvability. Future tests of this hypothesis should use G-matrices in a variety of wild organisms experiencing selection due to extreme climatic events.

Chromosome-scale genome assembly of the brown anole (Anolis sagrei), an emerging model species.

Rapid technological improvements are democratizing access to high quality, chromosome-scale genome assemblies. No longer the domain of only the most highly studied model organisms, now non-traditional and emerging model species can be genome-enabled using a combination of sequencing technologies and assembly software. Consequently, old ideas built on sparse sampling across the tree of life have recently been amended in the face of genomic data drawn from a growing number of high-quality reference genomes. Arguably the most valuable are those long-studied species for which much is already known about their biology; what many term emerging model species. Here, we report a highly complete chromosome-scale genome assembly for the brown anole, Anolis sagrei - a lizard species widely studied across a variety of disciplines and for which a high-quality reference genome was long overdue. This assembly exceeds the vast majority of existing reptile and snake genomes in contiguity (N50 = 253.6 Mb) and annotation completeness. Through the analysis of this genome and population resequence data, we examine the history of repetitive element accumulation, identify the X chromosome, and propose a hypothesis for the evolutionary history of fusions between autosomes and the X that led to the sex chromosomes of A. sagrei.

Dewlap colour variation in Anolis sagrei is maintained among habitats within islands of the West Indies.

Animal signals evolve in an ecological context. Locally adapting animal sexual signals can be especially important for initiating or reinforcing reproductive isolation during the early stages of speciation. Previous studies have demonstrated that dewlap colour in Anolis lizards can be highly variable between populations in relation to both biotic and abiotic adaptive drivers at relatively large geographical scales. Here, we investigated differentiation of dewlap coloration among habitat types at a small spatial scale, within multiple islands of the West Indies, to test the hypothesis that similar local adaptive processes occur over smaller spatial scales. We explored variation in dewlap coloration in the most widespread species of anole, Anolis sagrei, across three characteristic habitats spanning the Bahamas and the Cayman Islands, namely beach scrub, primary coppice forest and mangrove forest. Using reflectance spectrometry paired with supervised machine learning, we found significant differences in spectral properties of the dewlap between habitats within small islands, sometimes over very short distances. Passive divergence in dewlap phenotype associated with isolation-by-distance did not seem to explain our results. On the other hand, these habitat-specific dewlap differences varied in magnitude and direction across islands, and thus, our primary test for adaptation-parallel responses across islands-was not supported. We suggest that neutral processes or selection could be involved in several ways, including sexual selection. Our results shed new light on the scale at which signal colour polymorphism can be maintained in the presence of gene flow, and the relative role of local adaptation and other processes in driving these patterns of dewlap colour variation across islands.

When adaptive radiations collide: Different evolutionary trajectories between and within island and mainland lizard clades.

Oceanic islands are known as test tubes of evolution. Isolated and colonized by relatively few species, islands are home to many of nature's most renowned radiations from the finches of the Galápagos to the silverswords of the Hawaiian Islands. Despite the evolutionary exuberance of insular life, island occupation has long been thought to be irreversible. In particular, the presumed much tougher competitive and predatory milieu in continental settings prevents colonization, much less evolutionary diversification, from islands back to mainlands. To test these predictions, we examined the ecological and morphological diversity of neotropical Anolis lizards, which originated in South America, colonized and radiated on various islands in the Caribbean, and then returned and diversified on the mainland. We focus in particular on what happens when mainland and island evolutionary radiations collide. We show that extensive continental radiations can result from island ancestors and that the incumbent and invading mainland clades achieve their ecological and morphological disparity in very different ways. Moreover, we show that when a mainland radiation derived from island ancestors comes into contact with an incumbent mainland radiation the ensuing interactions favor the island-derived clade.

Adaptive Evolution in Cities: Progress and Misconceptions.

Current narratives suggest that urban adaptation - the adaptive evolution of organisms to cities - is pervasive across taxa and cities. However, in reviewing hundreds of studies, we find only six comprehensive examples of species adaptively evolving to urbanization. We discuss the utility and shortcomings of methods for studying urban adaptation. We then review diverse systems offering preliminary evidence for urban adaptation and outline a research program for advancing its study. Urban environments constitute diverse, interacting selective agents that test the limits of adaptation. Understanding urban adaptation therefore offers unique opportunities for addressing fundamental questions in evolutionary biology and for better conserving biodiversity in cities. However, capitalizing on these opportunities requires appropriate research methods and dissemination of accurate narratives.

Population increase and changes in behavior and morphology in the Critically Endangered Redonda ground lizard (Pholidoscelis atratus) following the successful removal of alien rats and goats.

Redonda is a small volcanic Caribbean island that is home to at least 4 endemic lizard species, including the Critically Endangered ground lizard (Pholidoscelis atratus). Black rats (Rattus rattus) and domestic goats (Capra hircus) were introduced to the island at some time after its discovery by Europeans in the late 1500s. They had a devastating effect on the island, resulting in the loss of nearly all trees and most of the ground vegetation. Point count surveys of P. atratus in 2012 indicated low densities, and the invasive rats were observed hunting and preying on the lizards. Both populations of rats and goats were successfully removed in 2017 as part of an ecological restoration program, and native vegetation and invertebrate populations have increased rapidly since. Population surveys in 2017, 2018, and 2019 show the lizard population has increased by more than sixfold. In 2017, as rats and goats were being removed, we evaluated the morphology and escape behavior of this species and repeated these measurements 1 year later. We observed that P. atratus had become bolder, with a reduced flight distance. We also detected changes in limb morphology related to locomotion and suggest possible explanations that will need to be further investigated in the future. These results show how the removal of invasive species can rapidly affect lizard population recovery and behavior, potentially restoring island ecosystems to their pre-human interference dynamics.

Trait differences among discrete morphs of a color polymorphic lizard, Podarcis erhardii.

Color polymorphism defies evolutionary expectations as striking phenotypic variation is maintained within a single species. Color and other traits mediate social interactions, and stable polymorphism within a population is hypothesized to be related to correlational selection of other phenotypic traits among color morphs. Here, we report on a previously unknown throat color polymorphism in the Aegean Wall Lizard (Podarcis erhardii) and examine morph-correlated differences in traits important to social behavior and communication: maximum bite force capacity and chemical signal profile. We find that both sexes of P. erhardii have three color morphs: orange, yellow, and white. Moreover, orange males are significantly larger and tend to bite harder than yellow and white males. Although the established color polymorphism only partially matches the observed intraspecific variation in chemical signal signatures, the chemical profile of the secretions of orange males is significantly divergent from that of white males. Our findings suggest that morph colors are related to differences in traits that are crucial for social interactions and competitive ability, illustrating the need to look beyond color when studying polymorphism evolution.

An extreme cold event leads to community-wide convergence in lower temperature tolerance in a lizard community.

Extreme climate events are predicted to increase in frequency and severity due to contemporary climate change. Recent studies have documented the evolutionary impacts of extreme events on single species, but no studies have yet investigated whether such events can drive community-wide patterns of trait shifts. On 22 January 2020, subtropical south Florida experienced an extreme cold episode during which air temperatures dropped below the lower thermal limit of resident lizard populations. In the week immediately after the cold event, we documented decreased lower thermal limits (CTmin) of six co-occurring lizard species that vary widely in ecology, body size and thermal physiology. Although cold tolerance of these species differed significantly before the cold snap, lizards sampled immediately after had converged on the same new, lower limit of thermal tolerance. Here, we demonstrate that extreme climate events can drive substantial and synchronous community-wide trait changes and provide evidence that tropical and subtropical ectotherms-often characterized as unable to withstand rapid changes in climatic conditions-can endure climatic conditions that exceed their physiological limits. Future studies investigating the mechanisms driving these trait shifts will prove valuable in understanding the ability of ectotherm communities to mitigate climate change.

Urban biodiversity management using evolutionary tools.

Cities are fully functioning ecosystems and are home to no-analogue communities of species that interact with each other and which are subject to novel urban stressors. As such, biodiversity can evolve in response to these new urban conditions, making urban species a moving target for conservation and management efforts. An evolving urban biodiversity necessitates integrating evolutionary insights into management for these efforts to be successful in a dynamic urban milieu. Here we present a framework for categorizing urban biodiversity from a management perspective. We then discuss a suite of example management tools and their potential evolutionary implications-both their opportunities for and potential consequence to management. Urban ecosystems are proliferating but, far from being ecological lost causes, they may provide unique insights and opportunities for biodiversity conservation. Determining how to achieve urban biodiversity priorities while managing pest species requires evolutionary thinking.

Rapid and repeated divergence of animal chemical signals in an island introduction experiment.

Studies of animal communication have documented myriad rapid, context-dependent changes in visual and acoustic signal design. In contrast, relatively little is known about the capacity of vertebrate chemical signals to rapidly respond, either plastically or deterministically, to changes in context. Four years following an experimental introduction of lizards to replicate experimental islets, we aimed to determine if chemical signal design of the experimental populations differed from that of the source population. In 2014, we translocated Podarcis erhardii lizards from a large, predator-rich island to each of five replicate predator-free islets. Mean population densities increased fivefold over the following 4 years and bite scars suggest significantly more intraspecific fighting among these experimental populations. In 2018, we analysed the chemical signal design of males in each of the experimental populations and compared it to the chemical signals of the source population. We found that males consistently presented a significantly more complex chemical signal compared to the source population. Moreover, their chemical signals were marked by high proportions of octadecanoic acid, oleic acid and α-tocopherol, the three compounds that are known to be associated with lizard territoriality and mate choice. Our island introduction experiment thus suggests that the chemical signal design of animals can shift rapidly and predictably in novel ecological contexts.

Hurricane effects on Neotropical lizards span geographic and phylogenetic scales.

Extreme climate events such as droughts, cold snaps, and hurricanes can be powerful agents of natural selection, producing acute selective pressures very different from the everyday pressures acting on organisms. However, it remains unknown whether these infrequent but severe disruptions are quickly erased by quotidian selective forces, or whether they have the potential to durably shape biodiversity patterns across regions and clades. Here, we show that hurricanes have enduring evolutionary impacts on the morphology of anoles, a diverse Neotropical lizard clade. We first demonstrate a transgenerational effect of extreme selection on toepad area for two populations struck by hurricanes in 2017. Given this short-term effect of hurricanes, we then asked whether populations and species that more frequently experienced hurricanes have larger toepads. Using 70 y of historical hurricane data, we demonstrate that, indeed, toepad area positively correlates with hurricane activity for both 12 island populations of Anolis sagrei and 188 Anolis species throughout the Neotropics. Extreme climate events are intensifying due to climate change and may represent overlooked drivers of biogeographic and large-scale biodiversity patterns.

Habitat shapes the thermoregulation of Mediterranean lizards introduced to replicate experimental islets.

Both environmental temperatures and spatial heterogeneity can profoundly affect the biology of ectotherms. In lizards, thermoregulation may show high plasticity and may respond to environmental shifts. In the context of global climate change, lizards showing plastic thermoregulatory responses may be favored. In this study, we designed an experiment to evaluate the extent to which lizard thermoregulation responds to introduction to a new environment in a snapshot of time. In 2014, we captured individuals of the Aegean Wall lizard (Podarcis erhardii) from Naxos Island (429.8 km2) and released them onto two small, lizard-free islets, Galiatsos (0.0073 km2) and Kampana (0.004 km2) (Aegean Sea, Greece). In 2017, we returned to the islets and estimated the effectiveness (E), accuracy and precision of thermoregulation measuring operative, preferred (Tpref) and body temperatures. We hypothesized that the three habitats would differ in thermal quality and investigated the extent to which lizards from Naxos demonstrate plasticity when introduced to the novel, islet habitats. Thermal parameters did not differ between Galiatsos and Naxos and this was reflected in the similar E and Tpref. However, lizards from Kampana deviated in all focal traits from Naxos, resulting in higher E and a preference for higher Tpref. In sum, Naxos lizards shifted their thermoregulatory profile due to the idiosyncratic features of their new islet habitat. Our results advocate a high plasticity in lizard thermoregulation and suggest that there is room for effective responses to environmental changes, at least for Podarcis lizards in insular habitats.

Hurricane-induced selection on the morphology of an island lizard.

Hurricanes are catastrophically destructive. Beyond their toll on human life and livelihoods, hurricanes have tremendous and often long-lasting effects on ecological systems1,2. Despite many examples of mass mortality events following hurricanes3-5, hurricane-induced natural selection has not previously been demonstrated. Immediately after we finished a survey of Anolis scriptus-a common, small-bodied lizard found throughout the Turks and Caicos archipelago-our study populations were battered by Hurricanes Irma and Maria. Shortly thereafter, we revisited the populations to determine whether morphological traits related to clinging capacity had shifted in the intervening six weeks and found that populations of surviving lizards differed in body size, relative limb length and toepad size from those present before the storm. Our serendipitous study, which to our knowledge is the first to use an immediately before and after comparison6 to investigate selection caused by hurricanes, demonstrates that hurricanes can induce phenotypic change in a population and strongly implicates natural selection as the cause. In the decades ahead, as extreme climate events are predicted to become more intense and prevalent7,8, our understanding of evolutionary dynamics needs to incorporate the effects of these potentially severe selective episodes9-11.

Aegean wall lizards switch foraging modes, diet, and morphology in a human-built environment.

Foraging mode is a functional trait with cascading impacts on ecological communities. The foraging syndrome hypothesis posits a suite of concurrent traits that vary with foraging mode; however, comparative studies testing this hypothesis are typically interspecific. While foraging modes are often considered typological for a species when predicting foraging-related traits or mode-specific cascading impacts, intraspecific mode switching has been documented in some lizards. Mode-switching lizards provide an opportunity to test foraging syndromes and explore how intraspecific variability in foraging mode might affect local ecological communities.Because lizard natural history is intimately tied to habitat use and structure, I tested for mode switching between populations of the Aegean wall lizard, Podarcis erhardii, inhabiting undisturbed habitat and human-built rock walls on the Greek island of Naxos. I observed foraging behavior among 10 populations and tested lizard morphological and performance predictions at each site. Furthermore, I investigated the diet of lizards at each site relative to the available invertebrate community.I found that lizards living on rock walls were significantly more sedentary-sit and wait-than lizards at nonwall sites. I also found that head width increased in females and the ratio of hindlimbs to forelimbs in both sexes increased as predicted. Diet also changed, with nonwall lizards consuming a higher proportion of sedentary prey. Lizard bite force also varied significantly between sites; however, the pattern observed was opposite to that predicted, suggesting that bite force in these lizards may more closely relate to intraspecific competition than to diet.This study demonstrates microgeographic variability in lizard foraging mode as a result of human land use. In addition, these results demonstrate that foraging mode syndromes can shift intraspecifically with potential cascading effects on local ecological communities.

Adaptive evolution in urban ecosystems.

Urban ecologists have demonstrated that cities are functioning ecosystems. It follows then that species living in these contexts should participate in and experience the same suite of biological processes, including evolution, that have occupied scientists for centuries in more "natural" contexts. In fact, urban ecosystems with myriad novel contexts, pressures, and species rosters provide unprecedentedly potent evolutionary stimuli. Here, we present the case for studying adaptive evolution in urban settings. We then review and synthesize techniques into a coherent approach for studying adaptive evolution in urban settings that combines observations of phenotypic divergence, measurements of fitness benefits of novel genetically based phenotypes, and experimental manipulations of potential drivers of adaptation. We believe that studying evolution in urban contexts can provide insights into fundamental evolutionary biology questions on rate, direction, and repeatability of evolution, and may inform species and ecosystem service conservation efforts.