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.

Predator-induced collapse of niche structure and species coexistence.

Biological invasions are both a pressing environmental challenge and an opportunity to investigate fundamental ecological processes, such as the role of top predators in regulating biodiversity and food-web structure. In whole-ecosystem manipulations of small Caribbean islands on which brown anole lizards (Anolis sagrei) were the native top predator, we experimentally staged invasions by competitors (green anoles, Anolis smaragdinus) and/or new top predators (curly-tailed lizards, Leiocephalus carinatus). We show that curly-tailed lizards destabilized the coexistence of competing prey species, contrary to the classic idea of keystone predation. Fear-driven avoidance of predators collapsed the spatial and dietary niche structure that otherwise stabilized coexistence, which intensified interspecific competition within predator-free refuges and contributed to the extinction of green-anole populations on two islands. Moreover, whereas adding either green anoles or curly-tailed lizards lengthened food chains on the islands, adding both species reversed this effect-in part because the apex predators were trophic omnivores. Our results underscore the importance of top-down control in ecological communities, but show that its outcomes depend on prey behaviour, spatial structure, and omnivory. Diversity-enhancing effects of top predators cannot be assumed, and non-consumptive effects of predation risk may be a widespread constraint on species coexistence.

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.

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.

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.

Effects of size selection versus density dependence on life histories: A first experimental probe.

When prey experience size-based harvesting by predators, they are not only subject to selection due to larger individuals being preferentially harvested but also selection due to reductions in population density. Density-dependent selection represents one of the most basic interactions between ecology and evolution. Yet, the reduction in density associated with exploitation has not been tested as a possible driving force of observed evolutionary changes in populations harvested size-dependently. Using an artificial selection experiment with a mixture of Daphnia clones, we partition the evolutionary effects of size-based harvesting into the effects of removing large individuals and the effects of lowering the population density. We show that both size selection and density-dependent selection are significant drivers of life-history evolution. Importantly, these drivers affected different life-history traits with size-selective harvesting selecting for slower juvenile growth rates and a larger size at maturity, and low-density selecting for reduced reproductive output.

Consumer Responses to Experimental Pulsed Subsidies in Isolated versus Connected Habitats.

AbstractIncreases in consumer abundance following a resource pulse can be driven by diet shifts, aggregation, and reproductive responses, with combined responses expected to result in faster response times and larger numerical increases. Previous work in plots on large Bahamian islands has shown that lizards (Anolis sagrei) increased in abundance following pulses of seaweed deposition, which provide additional prey (i.e., seaweed detritivores). Numerical responses were associated with rapid diet shifts and aggregation, followed by increased reproduction. These dynamics are likely different on isolated small islands, where lizards cannot readily immigrate or emigrate. To test this, we manipulated the frequency and magnitude of seaweed resource pulses on whole small islands and in plots within large islands, and we monitored lizard diet and numerical responses over 4 years. We found that seaweed addition caused persistent increases in lizard abundance on small islands regardless of pulse frequency or magnitude. Increased abundance may have occurred because the initial pulse facilitated population establishment, possibly via enhanced overwinter survival. In contrast with a previous experiment, we did not detect numerical responses in plots on large islands, despite lizards consuming more marine resources in subsidized plots. This lack of a numerical response may be due to rapid aggregation followed by disaggregation or to stronger suppression of A. sagrei by their predators on the large islands in this study. Our results highlight the importance of habitat connectivity in governing ecological responses to resource pulses and suggest that disaggregation and changes in survivorship may be underappreciated drivers of pulse-associated dynamics.

Lizards on newly created islands independently and rapidly adapt in morphology and diet.

Rapid adaptive changes can result from the drastic alterations humans impose on ecosystems. For example, flooding large areas for hydroelectric dams converts mountaintops into islands and leaves surviving populations in a new environment. We report differences in morphology and diet of the termite-eating gecko Gymnodactylus amarali between five such newly created islands and five nearby mainland sites located in the Brazilian Cerrado, a biodiversity hotspot. Mean prey size and dietary prey-size breadth were larger on islands than mainlands, expected because four larger lizard species that also consume termites, but presumably prefer larger prey, went extinct on the islands. In addition, island populations had larger heads relative to their body length than mainland populations; larger heads are more suited to the larger prey taken, and disproportionately larger heads allow that functional advantage without an increase in energetic requirements resulting from larger body size. Parallel morphological evolution is strongly suggested, because there are indications that, before flooding, relative head size did not differ between future island and future mainland sites. Females and males showed the same trend of relatively larger heads on islands, so the difference between island and mainland sites is unlikely to be due to greater male-male competition for mates on islands. We thus discovered a very fast (at most 15 y) case of independent parallel adaptive change in response to catastrophic human disturbance.

Pulsed seaweed subsidies drive sequential shifts in the effects of lizard predators on island food webs.

Most prominent theories of food web dynamics imply the simultaneous action of bottom-up and top-down forces. However, transient bottom-up effects resulting from resource pulses can lead to sequential shifts in the strength of top-down predator effects. We used a large-scale field experiment (32 small islands sampled over 5 years) to probe how the frequency and magnitude of pulsed seaweed inputs drives temporal variation in the top-down effects of lizard predators. Short-term weakening of lizard effects on spiders and plants (the latter via a trophic cascade) were associated with lizard diet shifts, and were more pronounced with larger seaweed inputs. Long-term strengthening of lizard effects was associated with lizard numerical responses and plant fertilisation. Increased pulse frequency reinforced the strengthening of lizard effects on spiders and plants. These results underscore the temporally variable nature of top-down effects and highlight the role of resource pulses in driving this variation.

Predation-associated modulation of movement-based signals by a Bahamian lizard.

Signaling individuals must effectively capture and hold the attention of intended conspecific receivers while limiting eavesdropping by potential predators. A possible mechanism for achieving this balance is for individuals to modulate the physical properties of their signals or to alter the proportion of time spent signaling, depending upon local levels of predation pressure. We test the hypothesis that prey can alter their visual signaling behavior to decrease conspicuousness and potentially limit predation risk via modulation of signal properties or display rate. To do so, we conducted a manipulative experiment in nature to evaluate the possible effect of predation pressure on the physical properties of movement-based signals and on the proportion of time spent signaling by using a well-understood predator-prey system in the Bahamas, the semiarboreal lizard Anolis sagrei, and one of its main predators, the curly-tailed lizard Leiocephalus carinatus. We find that on islands onto which the predator was introduced, male anoles reduce the maximum amplitude of head-bob displays but not the proportion of time spent signaling, in comparison with control islands lacking the predator. This reduction of amplitude also decreases signal active space, which might alter the reproductive success of signaling individuals. We suggest that future studies of predator-prey interactions consider the risk effects generated by changes in signals or signaling behavior to fully determine the influence of predation pressure on the dynamics of prey populations.

Predators suppress herbivore outbreaks and enhance plant recovery following hurricanes.

Understanding processes that may stabilize ecological systems confronted with rapidly changing environmental conditions is a key issue in ecology. We studied a system of highly fluctuating populations, the moth Achyra rantalis feeding on the plant Sesuvium portulacastrum in a group of small subtropical islands of the Bahamas. The plant is a prostrate inhabitant of shorelines, and consequently moths are highly vulnerable to being consumed by the ground-foraging lizard Anolis sagrei. We measured the percent ground cover of Sesuvium and abundance of Achyra on 11 islands with lizards present and 21 islands without lizards annually for 10 consecutive years. Overall abundance of Achyra was 4.6 times higher on no-lizard islands than on lizard islands. The percent cover of Sesuvium exhibited lower temporal variability on lizard islands when the study site was undisturbed by hurricanes, and higher recovery rate on lizard islands following hurricanes. We suggest that both of these stabilizing phenomena are linked to a trophic cascade in which predatory lizards control herbivore populations, thereby suppressing outbreaks and enhancing plant recovery following physical disturbance.

Mechanisms causing variation in sexual size dimorphism in three sympatric, congeneric lizards.

Sexual differences in adult body size (sexual size dimorphism, or SSD) ultimately can be favored by selection because larger males are more likely to be successful competitors for females, because larger females bear larger clutches, or because intersexual size differences reduce resource competition. Natural selection during juvenile development can influence sexual dimorphism of adults, and selection on adults and juveniles may differ. Studies that address the relative contributions of adult body shape dimorphism and sexually dimorphic patterns of growth and maturity are particularly useful in understanding the evolution of size dimorphism, yet they are rare. We investigated three sympatric, congeneric lizard species with different degrees and directions of adult sexual dimorphism and compared their growth patterns, survival probabilities, and intersexual trophic niche differences. Different mechanisms, even within these closely related, sympatric species, acted on juvenile lizards to produce species differences in adult SSD. Both degree and direction of dimorphism resulted from differences between the sexes in either the duration of growth or the rate of growth, but not from differences in rates of survival or selection on juvenile growth rate. Species- and sex-specific trade-offs in the allocation of energy to growth and reproduction, as well as differential timing of maturation, thus caused the growth patterns of the sexes to diverge, producing SSD. The differences that we observed in the direction of SSD among these species is consistent with their different social systems, suggesting that differential selection on adult body size has been responsible for the observed species-specific differences in juvenile growth rates and maturational timing.

The effect of chronic seaweed subsidies on herbivory: plant-mediated fertilization pathway overshadows lizard-mediated predator pathways.

Flows of energy and materials link ecosystems worldwide and have important consequences for the structure of ecological communities. While these resource subsidies typically enter recipient food webs through multiple channels, most previous studies focussed on a single pathway of resource input. We used path analysis to evaluate multiple pathways connecting chronic marine resource inputs (in the form of seaweed deposits) and herbivory in a shoreline terrestrial ecosystem. We found statistical support for a fertilization effect (seaweed increased foliar nitrogen content, leading to greater herbivory) and a lizard numerical response effect (seaweed increased lizard densities, leading to reduced herbivory), but not for a lizard diet-shift effect (seaweed increased the proportion of marine-derived prey in lizard diets, but lizard diet was not strongly associated with herbivory). Greater seaweed abundance was associated with greater herbivory, and the fertilization effect was larger than the combined lizard effects. Thus, the bottom-up, plant-mediated effect of fertilization on herbivory overshadowed the top-down effects of lizard predators. These results, from unmanipulated shoreline plots with persistent differences in chronic seaweed deposition, differ from those of a previous experimental study of the short-term effects of a pulse of seaweed deposition: while the increase in herbivory in response to chronic seaweed deposition was due to the fertilization effect, the short-term increase in herbivory in response to a pulse of seaweed deposition was due to the lizard diet-shift effect. This contrast highlights the importance of the temporal pattern of resource inputs in determining the mechanism of community response to resource subsidies.

Differential genotype response to increased resource abundance helps explain parallel evolution of Daphnia populations in the wild.

Under controlled laboratory conditions, previous studies have shown that selection can produce repeatable evolutionary trajectories. Yet, the question remains for many of these studies if, given identical starting populations, evolution in the wild proceeds in a non-random direction. In the present study, we investigated the extent to which rapid evolution in the wild is parallel by monitoring the genetic composition of replicate populations of Daphnia in field mesocosms containing two clonal genotypes. We found parallel changes across all nine mesocosms, in which the same genotype increased in frequency. To probe whether genotype-specific response to resource abundance could have led to this frequency change, we conducted a life-history assay under high-resource abundance and low-resource abundance. We found that resource exploitation differed by genotype, in that, while one genotype (the winner in the field mesocosms) was more fit than the other genotype at high resources, the other genotype performed slightly better at low resources. We suspect that levels of resource abundance found in the summer field mesocosms had values in which the genotype better with abundant resources had the advantage. These findings suggest that variation in certain traits associated with resource acquisition can drive genotype frequency change.

Predators determine how weather affects the spatial niche of lizard prey: exploring niche dynamics at a fine scale.

Although abiotic and biotic factors can interact to shape the spatial niche of a species, studies that explore the interactive effects of both at a local scale are rare. We demonstrate that one of the main axes (perch height) characterizing the spatial niche of a common lizard, Anolis sagrei, varies according to the interactive effects of weather and the activity of a larger predatory lizard, Leiocephalus carinatus. Results were completely consistent: no matter how favorable the weather conditions for using the ground (mainly characterized by temperature, humidity, wind speed, rain), A. sagrei did not do so if the predator was present. Hence, great behavioral plasticity enabled A. sagrei to adjust its use of space very quickly. To the best of our knowledge, these results constitute the first field demonstration for anoles (and possibly for other animals as well) of how time-varying environmental conditions and predator presence interact to produce short-term changes in utilization along a major niche axis.

Self-made shelters protect spiders from predation.

Many animals modify their environments, apparently to reduce predation risk, but the success of such endeavors, and their impact on the density and distribution of populations, are rarely rigorously demonstrated. We staged a manipulative experiment to assess the effectiveness of self-made shelters by web spiders as protection from natural enemies. Scincid lizards were included or excluded from 21 replicated 200-m(2) plots, and spiders therein were classified as exposed or sheltered, depending on whether they were uncovered in their web or hidden in cocoons, leaves/debris, or burrows. We found that exposed spiders were greatly affected by the presence of predatory scincid lizards, whereas sheltered spiders were not. More specifically, lizards, which forage close to the ground, reduced the abundance of exposed spiders by two-thirds but had no effect on the abundance of sheltered spiders. Sheltered spiders were able to avoid predation and share space with lizards, suggesting that shelter construction is a mechanism for reducing predation risk and has important population consequences.

Marine subsidies have multiple effects on coastal food webs.

The effect of resource subsidies on recipient food webs has received much recent attention. The purpose of this study was to measure the effects of significant seasonal seaweed deposition events, caused by hurricanes and other storms, on species inhabiting subtropical islands. The seaweed represents a pulsed resource subsidy that is consumed by amphipods and flies, which are eaten by lizards and predatory arthropods, which in turn consume terrestrial herbivores. Additionally, seaweed decomposes directly into the soil under plants. We added seaweed to six shoreline plots and removed seaweed from six other plots for three months; all plots were repeatedly monitored for 12 months after the initial manipulation. Lizard density (Anolis sagrei) responded rapidly, and the overall average was 63% higher in subsidized than in removal plots. Stable-isotope analysis revealed a shift in lizard diet composition toward more marine-based prey in subsidized plots. Leaf damage was 70% higher in subsidized than in removal plots after eight months, but subsequent damage was about the same in the two treatments. Foliage growth rate was 70% higher in subsidized plots after 12 months. Results of a complementary study on the relationship between natural variation in marine subsidies and island food web components were consistent with the experimental results. We suggest two causal pathways for the effects of marine subsidies on terrestrial plants: (1) the "fertilization effect" in which seaweed adds nutrients to plants, increasing their growth rate, and (2) the "predator diet shift effect" in which lizards shift from eating local prey (including terrestrial herbivores) to eating mostly marine detritivores.

Predator-induced behaviour shifts and natural selection in field-experimental lizard populations.

The role of behaviour in evolutionary change has long been debated. On the one hand, behavioural changes may expose individuals to new selective pressures by altering the way that organisms interact with the environment, thus driving evolutionary divergence. Alternatively, behaviour can act to retard evolutionary change: by altering behavioural patterns in the face of new environmental conditions, organisms can minimize exposure to new selective pressures. This constraining influence of behaviour has been put forward as an explanation for evolutionary stasis within lineages and niche conservatism within clades. Nonetheless, the hypothesis that behavioural change prevents natural selection from operating in new environments has never been experimentally tested. We conducted a controlled and replicated experimental study of selection in entirely natural populations; we demonstrate that lizards alter their habitat use in the presence of an introduced predator, but that these behavioural shifts do not prevent patterns of natural selection from changing in experimental populations.

Population differences in aggression are shaped by tropical cyclone-induced selection.

Extreme events, such as tropical cyclones, are destructive and influential forces. However, observing and recording the ecological effects of these statistically improbable, yet profound 'black swan' weather events is logistically difficult. By anticipating the trajectory of tropical cyclones, and sampling populations before and after they make landfall, we show that these extreme events select for more aggressive colony phenotypes in the group-living spider Anelosimus studiosus. This selection is great enough to drive regional variation in colony phenotypes, despite the fact that tropical cyclone strikes are irregular, occurring only every few years, even in particularly prone regions. These data provide compelling evidence for tropical cyclone-induced selection driving the evolution of an important functional trait and show that black swan events contribute to within-species diversity and local adaptation.

Call-to-Action: A Global Consortium for Tropical Cyclone Ecology.

Rigorously evaluating of the ecological impacts of cyclones is logistically challenging. Here we issue a call-to-action to organize a global collaboration initiative to advance cyclone ecology. If successful, this will allow the international community to pose some of the most exciting questions in ecology and provide definitive answers.