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.

Fluctuating selection maintains distinct species phenotypes in an ecological community in the wild.

Species' phenotypic characteristics often remain unchanged over long stretches of geological time. Stabilizing selection-in which fitness is highest for intermediate phenotypes and lowest for the extremes-has been widely invoked as responsible for this pattern. At the community level, such stabilizing selection acting individually on co-occurring species is expected to produce a rugged fitness landscape on which different species occupy distinct fitness peaks. However, even with an explosion of microevolutionary field studies over the past four decades, evidence for persistent stabilizing selection driving long-term stasis is lacking. Nonetheless, biologists continue to invoke stabilizing selection as a major factor explaining macroevolutionary patterns. Here, by directly measuring natural selection in the wild, we identified a complex community-wide fitness surface in which four Anolis lizard species each occupy a distinct fitness peak close to their mean phenotype. The presence of local fitness optima within species, and fitness valleys between species, presents a barrier to adaptive evolutionary change and acts to maintain species differences through time. However, instead of continuously operating stabilizing selection, we found that species were maintained on these peaks by the combination of many independent periods among which selection fluctuated in form, strength, direction, or existence and in which stabilizing selection rarely occurred. Our results suggest that lack of substantial phenotypic evolutionary change through time may be the result of selection, but not persistent stabilizing selection as classically envisioned.

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.

How exceptional are the classic adaptive radiations of passerine birds?

We investigated whether celebrated cases of evolutionary radiations of passerine birds on islands have produced exceptional morphological diversity relative to comparable-aged radiations globally. Based on eight external measurements, we calculated the disparity in size and shape within clades, each of which was classified as being tropical or temperate and as having diversified in a continental or an island/archipelagic setting. We found that the distribution of disparity among all clades does not differ substantively from a normal distribution, which would be consistent with a common underlying process of morphological diversification that is largely independent of latitude and occurrence on islands. Disparity is slightly greater in island clades than in those from continents or clades consisting of island and noninsular taxa, revealing a small, but significant, effect of island occurrence on evolutionary divergence. Nonetheless, the number of highly disparate clades overall is no greater than expected from a normal distribution, calling into question the need to invoke key innovations, ecological opportunity, or other factors as stimuli for adaptive radiations in passerine birds.

When adaptation is slowed down: Genomic analysis of evolutionary stasis in thermal tolerance during biological invasion in a novel climate.

Research conducted during the past two decades has demonstrated that biological invasions are excellent models of rapid evolution. Even so, characteristics of invasive populations such as a short time for recombination to assemble optimal combinations of alleles may occasionally limit adaptation to new environments. Here, we investigated such genetic constraints to adaptation in the invasive brown anole (Anolis sagrei)-a tropical ectotherm that was introduced to the southeastern United States, a region with a much colder climate than in its native Caribbean range. We examined thermal physiology for 30 invasive populations and tested for a climatic cline in cold tolerance. Also, we used genomics to identify mechanisms that may limit adaptation. We found no support for a climatic cline, indicating that thermal tolerance did not shift adaptively. Concomitantly, population genomic results were consistent with the occurrence of recombination cold spots that comprise more than half of the genome and maintain long-range associations among alleles in invasive populations. These genomic regions overlap with both candidate thermal tolerance loci that we identified using a standard genome-wide association test. Moreover, we found that recombination cold spots do not have a large contribution to population differentiation in the invasive range, contrary to observations in the native range. We suggest that limited recombination is constraining the contribution of large swaths of the genome to adaptation in invasive brown anoles. Our study provides an example of evolutionary stasis during invasion and highlights the possibility that reduced recombination occasionally slows down adaptation in invasive populations.

Signal size allometry in Anolis lizard dewlaps.

Positive allometry of signalling traits has often been taken as evidence for sexual selection. However, few studies have explored interspecific differences in allometric scaling relationships among closely related species that vary in their degree of ecological similarity. Anolis lizards possess an elaborate retractable throat fan called a dewlap that is used for visual communication and differs greatly in size and colour among species. We observed that Anolis dewlaps demonstrate positive allometry: relative dewlap size increases with body size. We also observed that coexisting species are divergent in signal size allometries, while convergent species-similar in other aspects of ecology, morphology and behaviour-typically share similar dewlap allometric scaling relationships. These patterns suggest that dewlap scaling relationships may follow the same pattern as other traits in the anole radiation, where ecologically different sympatric species have evolved a suite of divergent traits.

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.

Urban evolutionary ecology brings exaptation back into focus.

The contribution of pre-existing phenotypic variation to evolution in novel environments has long been appreciated. Nevertheless, evolutionary ecologists have struggled with communicating these aspects of the adaptive process. In 1982, Gould and Vrba proposed terminology to distinguish character states shaped via natural selection for the roles they currently serve ('adaptations') from those shaped under preceding selective regimes ('exaptations'), with the intention of replacing the inaccurate 'preadaptation'. Forty years later, we revisit Gould and Vrba's ideas which, while often controversial, continue to be widely debated and highly cited. We use the recent emergence of urban evolutionary ecology as a timely opportunity to reintroduce the ideas of Gould and Vrba as an integrated framework to understand contemporary evolution in novel environments.

The Difficulty of Predicting Evolutionary Change in Response to Novel Ecological Interactions: A Field Experiment with Anolis Lizards.

AbstractDetermining whether and how evolution is predictable is an important goal, particularly as anthropogenic disturbances lead to novel species interactions that could modify selective pressures. Here, we use a multigeneration field experiment with brown anole lizards (Anolis sagrei) to test hypotheses about the predictability of evolution. We manipulated the presence/absence of predators and competitors of A. sagrei across 16 islands in the Bahamas that had preexisting brown anole populations. Before the experiment and again after roughly five generations, we measured traits related to locomotor performance and habitat use by brown anoles and used double-digest restriction enzyme-associated DNA sequencing to estimate genome-wide changes in allele frequencies. Although previous work showed that predators and competitors had characteristic effects on brown anole behavior, diet, and population sizes, we found that evolutionary change at both phenotypic and genomic levels was difficult to forecast. Phenotypic changes were contingent on sex and habitat use, whereas genetic change was unpredictable and not measurably correlated with phenotypic changes, experimental treatments, or other environmental factors. Our work shows how differences in ecological context can alter evolutionary outcomes over short timescales and underscores the difficulty of forecasting evolutionary responses to multispecies interactions in natural conditions, even in a well-studied system with ample supporting ecological information.

Introduction history and hybridization determine the hydric balance of an invasive lizard facing a recent climate niche shift.

As anthropogenic activities are increasing the frequency and severity of droughts, understanding whether and how fast populations can adapt to sudden changes in their hydric environment is critically important. Here, we capitalize on the introduction of the Cuban brown anole lizard (Anolis sagrei) in North America to assess the contemporary evolution of a widespread terrestrial vertebrate to an abrupt climatic niche shift. We characterized hydric balance in 30 populations along a large climatic gradient. We found that while evaporative and cutaneous water loss varied widely, there was no climatic cline, as would be expected under adaptation. Furthermore, the skin of lizards from more arid environments was covered with smaller scales, a condition thought to limit water conservation and thus be maladaptive. In contrast to environmental conditions, genome-averaged ancestry was a significant predictor of water loss. This was reinforced by our genome-wide association analyses, which indicated a significant ancestry-specific effect for water loss at one locus. Thus, our study indicates that the water balance of invasive brown anoles is dictated by an environment-independent introduction and hybridization history and highlights genetic interactions or genetic correlations as factors that might forestall adaptation. Alternative water conservation strategies, including behavioral mitigation, may influence the brown anole invasion success and require future examination.

Genome-wide parallelism underlies contemporary adaptation in urban lizards.

Urbanization drastically transforms landscapes, resulting in fragmentation, degradation, and the loss of local biodiversity. Yet, urban environments also offer opportunities to observe rapid evolutionary change in wild populations that survive and even thrive in these novel habitats. In many ways, cities represent replicated "natural experiments" in which geographically separated populations adaptively respond to similar selection pressures over rapid evolutionary timescales. Little is known, however, about the genetic basis of adaptive phenotypic differentiation in urban populations nor the extent to which phenotypic parallelism is reflected at the genomic level with signatures of parallel selection. Here, we analyzed the genomic underpinnings of parallel urban-associated phenotypic change in Anolis cristatellus, a small-bodied neotropical lizard found abundantly in both urbanized and forested environments. We show that phenotypic parallelism in response to parallel urban environmental change is underlain by genomic parallelism and identify candidate loci across the Anolis genome associated with this adaptive morphological divergence. Our findings point to polygenic selection on standing genetic variation as a key process to effectuate rapid morphological adaptation. Identified candidate loci represent several functions associated with skeletomuscular development, morphology, and human disease. Taken together, these results shed light on the genomic basis of complex morphological adaptations, provide insight into the role of contingency and determinism in adaptation to novel environments, and underscore the value of urban environments to address fundamental evolutionary questions.

The ecology and evolution of key innovations.

The idea of 'key innovations' has long been influential in theoretical and empirical approaches to understanding adaptive diversification. Despite originally revolving around traits inducing major ecological shifts, the key innovation concept itself has evolved, conflating lineage diversification with trait-dependent ecological shifts. In this opinion article we synthesize the history of the term, clarify the relationship between key innovations and adaptive radiation, and propose a return to the original concept of key innovations: the evolution of organismal features which permit a species to occupy a previously inaccessible ecological state. Ultimately, we suggest an integrative approach to studying key innovations, necessitating experimental approaches of form and function, natural history studies of resource use, and phylogenetic comparative perspectives.

Conservation and Convergence of Genetic Architecture in the Adaptive Radiation of Anolis Lizards.

AbstractThe G matrix, which quantifies the genetic architecture of traits, is often viewed as an evolutionary constraint. However, G can evolve in response to selection and may also be viewed as a product of adaptive evolution. Convergent evolution of G in similar environments would suggest that G evolves adaptively, but it is difficult to disentangle such effects from phylogeny. Here, we use the adaptive radiation of Anolis lizards to ask whether convergence of G accompanies the repeated evolution of habitat specialists, or ecomorphs, across the Greater Antilles. We measured G in seven species representing three ecomorphs (trunk-crown, trunk-ground, and grass-bush). We found that the overall structure of G does not converge. Instead, the structure of G is well conserved and displays a phylogenetic signal consistent with Brownian motion. However, several elements of G showed signatures of convergence, indicating that some aspects of genetic architecture have been shaped by selection. Most notably, genetic correlations between limb traits and body traits were weaker in long-legged trunk-ground species, suggesting effects of recurrent selection on limb length. Our results demonstrate that common selection pressures may have subtle but consistent effects on the evolution of G, even as its overall structure remains conserved.

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.

Changes in selection pressure can facilitate hybridization during biological invasion in a Cuban lizard.

Hybridization is among the evolutionary mechanisms most frequently hypothesized to drive the success of invasive species, in part because hybrids are common in invasive populations. One explanation for this pattern is that biological invasions coincide with a change in selection pressures that limit hybridization in the native range. To investigate this possibility, we studied the introduction of the brown anole (Anolis sagrei) in the southeastern United States. We find that native populations are highly genetically structured. In contrast, all invasive populations show evidence of hybridization among native-range lineages. Temporal sampling in the invasive range spanning 15 y showed that invasive genetic structure has stabilized, indicating that large-scale contemporary gene flow is limited among invasive populations and that hybrid ancestry is maintained. Additionally, our results are consistent with hybrid persistence in invasive populations resulting from changes in natural selection that occurred during invasion. Specifically, we identify a large-effect X chromosome locus associated with variation in limb length, a well-known adaptive trait in anoles, and show that this locus is often under selection in the native range, but rarely so in the invasive range. Moreover, we find that the effect size of alleles at this locus on limb length is much reduced in hybrids among divergent lineages, consistent with epistatic interactions. Thus, in the native range, epistasis manifested in hybrids can strengthen extrinsic postmating isolation. Together, our findings show how a change in natural selection can contribute to an increase in hybridization in invasive populations.

What Determines Paternity in Wild Lizards? A Spatiotemporal Analysis of Behavior and Morphology.

Mating behavior in animals can be understood as a sequence of events that begins with individuals encountering one another and ends with the production of offspring. Behavioral descriptions of animal interactions characterize early elements of this sequence, and genetic descriptions use offspring parentage to characterize the final outcome, with behavioral and physiological assessments of mates and mechanisms of copulation and fertilization comprising intermediate steps. However, behavioral and genetic descriptions of mating systems are often inconsistent with one another, complicating expectations for crucial aspects of mating biology, such as the presence of multiple mating. Here, we use behavioral and genetic data from a wild population of the lizard Anolis cristatellus to characterize female multiple mating and the potential for sexual selection through female mate choice in this species. We find that 48% of sampled females bore offspring sired by multiple males. Moreover, spatiotemporal proximity between males and females was associated with whether a male sired a female's offspring, and if yes, how many offspring he sired. Additionally, male body size, but not display behavior, was associated with reproductive outcomes for male-female pairs. While much remains to be learned about the mechanisms of mating and targets of sexual selection in A. cristatellus, it is clear that female multiple mating is a substantial component of this species' mating system in nature.

Sex-specific microhabitat use is associated with sex-biased thermal physiology in Anolis lizards.

If fitness optima for a given trait differ between males and females in a population, sexual dimorphism may evolve. Sex-biased trait variation may affect patterns of habitat use, and if the microhabitats used by each sex have dissimilar microclimates, this can drive sex-specific selection on thermal physiology. Nevertheless, tests of differences between the sexes in thermal physiology are uncommon, and studies linking these differences to microhabitat use or behavior are even rarer. We examined microhabitat use and thermal physiology in two ectothermic congeners that are ecologically similar but differ in their degree of sexual size dimorphism. Brown anoles (Anolis sagrei) exhibit male-biased sexual size dimorphism and live in thermally heterogeneous habitats, whereas slender anoles (Anolis apletophallus) are sexually monomorphic in body size and live in thermally homogeneous habitats. We hypothesized that differences in habitat use between the sexes would drive sexual divergence in thermal physiology in brown anoles, but not slender anoles, because male and female brown anoles may be exposed to divergent microclimates. We found that male and female brown anoles, but not slender anoles, used perches with different thermal characteristics and were sexually dimorphic in thermal tolerance traits. However, field-active body temperatures and behavior in a laboratory thermal arena did not differ between females and males in either species. Our results suggest that sexual dimorphism in thermal physiology can arise from phenotypic plasticity or sex-specific selection on traits that are linked to thermal tolerance, rather than from direct effects of thermal environments experienced by males and females.

The Evolution of 'Ecological Release' into the 21st Century.

Ecological release, originally conceived as niche expansion following a reduction in interspecific competition, may prompt invasion success, morphological evolution, speciation, and other ecological and evolutionary outcomes. However, the concept has not been recently reviewed. Here, we trace the study of 'ecological release' from its inception through the present day and find that current definitions are broad and highly varied. Viewing this development as a potential impediment to clear communication and hypothesis testing, we suggest a consensus definition for ecological release: niche expansions and shifts when a constraining interspecific interaction is reduced or removed. In rationalizing this definition, we highlight the various ways ecological release can unfold and address its potential evolutionary consequences.