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In recent years, biologists have increasingly recognized that evolutionary change can occur rapidly when natural selection is strong; thus, real-time studies of evolution can be used to test classic evolutionary hypotheses directly. One such hypothesis is that negative interactions between closely related species can drive phenotypic divergence. Such divergence is thought to be ubiquitous, though well-documented cases are surprisingly rare. On small islands in Florida, we found that the lizard Anolis carolinensis moved to higher perches following invasion by Anolis sagrei and, in response, adaptively evolved larger toepads after only 20 generations. These results illustrate that interspecific interactions between closely related species can drive evolutionary change on observable time scales.

Negative interactions between species can generate divergent selection that causes character displacement. However, other processes cause similar divergence. We use spatial and temporal replication across island populations of Anolis lizards to assess the importance of negative interactions in driving trait shifts. Previous work showed that the establishment of Anolis sagrei on islands drove resident Anolis carolinensis to perch higher and evolve larger toepads. To further test the interaction’s causality and predictability, we resurveyed a subset of islands nine years later. Anolis sagrei had established on one island between surveys. We found that A. carolinensis on this island now perch higher and have larger toepads. However, toepad morphology change on this island was not distinct from shifts on six other islands whose Anolis community composition had not changed. Thus, the presence of A. sagrei only partly explains A. carolinensis trait variation across space and time. We also found that A. carolinensis on islands with previously established A. sagrei now perch higher than a decade ago, and that current A. carolinensis perch height is correlated with A. sagrei density. Our results suggest that character displacement likely interacts with other evolutionary processes in this system, and that temporal data are key to detecting such interactions.

Tropical ectotherms are thought to be especially vulnerable to climate change because they are adapted to relatively stable temperature regimes, such that even small increases in environmental temperature may lead to large decreases in physiological performance. One way in which tropical organisms may mitigate the detrimental effects of warming is through evolutionary change in thermal physiology. The speed and magnitude of this response depend, in part, on the strength of climate-driven selection. However, many ectotherms use behavioral adjustments to maintain preferred body temperatures in the face of environmental variation. These behaviors may shelter individuals from natural selection, preventing evolutionary adaptation to changing conditions. Here, we mimic the effects of climate change by experimentally transplanting a population of Anolis sagrei lizards to a novel thermal environment. Transplanted lizards experienced warmer and more thermally variable conditions, which resulted in strong directional selection on thermal performance traits. These same traits were not under selection in a reference population studied in a less thermally stressful environment. Our results indicate that climate change can exert strong natural selection on tropical ectotherms, despite their ability to thermoregulate behaviorally. To the extent that thermal performance traits are heritable, populations may be capable of rapid adaptation to anthropogenic warming. Significance Tropical ectotherms are considered especially vulnerable to climate change because they have narrow thermal tolerance ranges, such that even small increases in environmental temperature are likely to be detrimental. Although evolutionary adaptation may prevent extinction, it is unclear whether climate change generates selection on thermal physiology in nature or whether the strength of this selection is sufficient for rapid evolution to occur. When we transplanted lizards from their preferred habitat to a warmer and more thermally variable site, strong natural selection favored individuals that ran faster at warmer temperatures and across a broader range of temperatures. If thermal performance traits are heritable, some tropical species may be capable of rapid evolutionary adaptation to changing climates.

The evolution of sexual dimorphism is predicted to occur through reductions in between-sex genetic correlations (r mf) for shared traits, but the physiological and genetic mechanisms that facilitate these reductions remain largely speculative. Here, we use a paternal half-sibling breeding design in captive brown anole lizards (Anolis sagrei) to show that the development of sexual size dimorphism is mirrored by the ontogenetic breakdown of r mf for body size and growth rate. Using transcriptome data from the liver (which integrates growth and metabolism), we show that sex-biased gene expression also increases dramatically between ontogenetic stages bracketing this breakdown of r mf. Ontogenetic increases in sex-biased expression are particularly evident for genes involved in growth, metabolism, and cell proliferation, suggesting that they contribute to both the development of sexual dimorphism and the breakdown of r mf. Mechanistically, we show that treatment of females with testosterone stimulates the expression of male-biased genes while inhibiting the expression of female-biased genes, thereby inducing male-like phenotypes at both organismal and transcriptomic levels. Collectively, our results suggest that sex-specific modifiers such as testosterone can orchestrate sex-biased gene expression to facilitate the phenotypic development of sexual dimorphism while simultaneously reducing genetic correlations that would otherwise constrain the independent evolution of the sexes.

Founder populations often show rapid divergence from source populations after colonizing new environments. Epigenetic modifications can mediate phenotypic responses to environmental change and may be an important mechanism promoting rapid differentiation in founder populations. Whereas many long-term studies have explored the extent to which divergence between source and founder populations is genetically heritable versus plastic, the role of epigenetic processes during colonization remains unclear. To investigate epigenetic modifications in founding populations, we experimentally colonized eight small Caribbean islands with brown anole lizards (Anolis sagrei) from a common source population. We then quantitatively measured genome-wide DNA methylation in liver tissue using reduced representation bisulfite sequencing of individuals transplanted onto islands with high- versus low-habitat quality. We found that lizard sex and habitat quality explained a significant proportion of epigenetic variation. Differentially methylated cytosines mapped to genes that encode proteins with functions likely to be relevant to habitat change (e.g., signal transduction, immune response, circadian rhythm). This study provides experimental evidence of a relationship between epigenetic responses and the earliest stages of colonization of novel environments in nature and suggests that habitat quality influences the nature of these epigenetic modifications.

Native species can coexist with invasive congeners by partitioning niche space; however, impacts from invasive species often occur alongside other disturbances. Native species’ responses to the interactions of multiple disturbances remain poorly understood. Here we study the impacts of urbanization and an invasive congener on a native species. Using abundance (catch-per-unit effort) and vertical distribution of native green anoles (Anolis carolinensis) and invasive brown anoles (Anolis sagrei) across a gradient of natural-to-urban forests, we ask if niche shifting (lability) is occurring, and if it can mitigate impacts from one or both disturbances. We use generalized linear models to relate species abundances across the landscape to urbanization, forest structural complexity, and congener abundances (i.e., A. sagrei); and test for an interaction between urbanization and congener abundance. Our data show that A. sagrei presence results in a 17-fold upward shift in vertical niche of A. carolinensis—an 8.3 m shift in median perch height, and models reveal urbanization also drives an increase in A. carolinensis perch height. A. carolinensis and A. sagrei abundances negatively and positively correlate with urbanization, respectively, and neither species’ abundance correlate with congener abundance. Despite a positive correlation between A. sagrei abundance and urbanization, our results do not show evidence of this interaction affecting A. carolinensis. Instead, niche lability appears to enable the native species to mitigate the impact of one driver of decline (invasive competition) while our data suggest it declines with the second (urbanization).

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.

In the study of the evolution of animal colors, the conspicuousness of a pair of colors (e.g., stimulus vs. background) is often modeled by determining the distance between them in perceptual color space. For similar colors, receptor noise models have been demonstrated to be an effective way to estimate discrimination thresholds. However, the best way to quantify conspicuousness of color pairs that are distant in perceptual space is not widely agreed upon. In experiments where an animal is presented with different colors that it can easily discriminate, its response may be strongly influenced by the biological significance of a color, in addition to its conspicuousness, a phenomenon known as color categorization. This has made it difficult to test and confirm the validity of different models of perceptual distance. We tested the relative conspicuousness of different stimulus/background color combinations in the lizard Anolis sagrei using a visual attention reflex, which has been shown in earlier experiments to be less influenced by color categorization than other commonly used behavioral assays. We compared the results to predictions based on two different visual system-based models. The Euclidian distance between pairs of points plotted in a lizard chromaticity diagram effectively predicted the relative responses. A receptor noise model, in which color space distance was estimated in units of “just noticeable difference,” yielded a similarly accurate prediction of the results. We concluded that for studies of color signal evolution, either of these methods may be effectively employed to make behaviorally-relevant predictions of perceptual distance among colors that are widely separated in visual space.

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. Summary Sentence Two volumetric imaging modalities, contrast-enhanced micro-computed tomography and optical coherence tomography, facilitate visualization of the macro- and micro- architecture of the reproductive tract of the female brown anole, Anolis sagrei. Graphical Abstract

Nesting behavior is an important part of reproduction that affects maternal fitness. Females of most oviparous species choose microhabitats for nesting that have positive effects on embryo development. However, choosing suitable nest microhabitats could be challenging in environments that fluctuate unpredictably. In many reptiles, females avoid nesting in dry microhabitats because eggs rapidly desiccate. In nature, however, microhabitats with suitable hydric conditions at the time of oviposition may eventually become lethally dry during incubation. We designed an experiment to test whether female lizards (Anolis sagrei) avoid nesting in locations with unpredictable fluctuations in substrate moisture and choose sites with stable moist conditions. We provided captive lizards three nest conditions to choose among: 1) substrate that predictably alternated between suitable and lethal moisture conditions, 2) substrate that fluctuated unpredictably between suitable and lethal conditions, and 3) substrate with moisture levels that remained constant. For the constant choice, some females could choose moist substrate (which is suitable for embryos), and others could choose dry substrate (which rapidly desiccates eggs). Females always nested in substrates that were moist at the time of oviposition, regardless of the level of predictability. Additionally, while constantly dry substrate was avoided, females did not distinguish between predictable and unpredictable options, both of which resulted in 100% egg mortality. These results suggest that nest site choice is based on immediate environmental cues, rather than the level of predictability of future conditions of nest sites, which in turn can have negative consequences when environments fluctuate between suitable and unsuitable conditions.Significance statementFluctuating environments pose challenges to females when seeking suitable locations for laying eggs. Female brown anole lizards choose moist nest conditions that facilitate embryo development. However, because moisture levels of nest substrate can unpredictably change, females that avoid nesting in microhabitats with unpredictable moisture fluctuations may have increased fitness. We tested the ability of females to select sites based on moisture predictability by providing them with options where substrate moisture remained stable, fluctuated predictably, and fluctuated unpredictably. Females did not discriminate among stable and fluctuating substrates. Rather, they always nested in moist substrates that were present at the time of oviposition, even if their nest site eventually fluctuated towards lethally dry conditions. Our results show that extreme fluctuations lead to poor choices of nest sites, which is problematic under global change where fluctuations in ambient conditions are expected to increase.