Habitat choice stabilizes metapopulation dynamics by enabling ecological specialization

Dispersal is a key trait responsible for the spread of individuals and genes among local populations, thereby generating eco‐evolutionary interactions. Especially in heterogeneous metapopulations, a tight coupling between dispersal, population dynamics and the evolution of local adaptation is expected. In this respect, dispersal should counteract ecological specialization by redistributing locally selected phenotypes (i.e. migration load). Habitat choice following an informed dispersal decision, however, can facilitate the evolution of ecological specialization. How such informed decisions influence metapopulation size and variability is yet to be determined. By means of individual‐based modelling, we demonstrate that informed decisions about both departure and settlement decouple the evolution of dispersal and that of generalism, selecting for highly dispersive specialists. Choice at settlement is based on information from the entire dispersal range, and therefore decouples dispersal from ecological specialization more effectively than choice at departure, which is only based on local information. Additionally, habitat choice at departure and settlement reduces local and metapopulation variability because of the maintenance of ecological specialization at all levels of dispersal propensity. Our study illustrates the important role of habitat choice for dynamics of spatially structured populations and thus emphasizes the importance of considering that dispersal is often informed.     

Eco-evolutionary feedback and the invasion of cooperation in prisoner's dilemma games

Unveiling the origin and forms of cooperation in nature poses profound challenges in evolutionary ecology. The prisoner's dilemma game is an important metaphor for studying the evolution of cooperation. We here classified potential mechanisms for cooperation evolution into schemes of frequency- and density-dependent selection, and focused on the density-dependent selection in the ecological prisoner's dilemma games. We found that, although assortative encounter is still the necessary condition in ecological games for cooperation evolution, a harsh environment, indicated by a high mortality, can foster the invasion of cooperation. The Hamilton rule provides a fundamental condition for the evolution of cooperation by ensuring an enhanced relatedness between players in low-density populations. Incorporating ecological dynamics into evolutionary games opens up a much wider window for the evolution of cooperation, and exhibits a variety of complex behaviors of dynamics, such as limit and heteroclinic cycles. An alternative evolutionary, or rather succession, sequence was proposed that cooperation first appears in harsh environments, followed by the invasion of defection, which leads to a common catastrophe. The rise of cooperation (and altruism), thus, could be much easier in the density-dependent ecological games than in the classic frequency-dependent evolutionary games.     

A newly discovered role of evolution in previously published consumer–resource dynamics

Consumer–resource interactions are fundamental components of ecological communities. Classic features of consumer–resource models are that temporal dynamics are often cyclic, with a ¼‐period lag between resource and consumer population peaks. However, there are few published empirical examples of this pattern. Here, we show that many published examples of consumer–resource cycling show instead patterns indicating eco‐evolutionary dynamics. When prey evolve along a trade‐off between defence and competitive ability, two‐species consumer–resource cycles become longer and antiphase (half‐period lag, so consumer maxima coincide with minima of the resource species). Using stringent criteria, we identified 21 two‐species consumer–resource time series, published between 1934 and 1997, suitable to investigate for eco‐evolutionary dynamics. We developed a statistical method to probe for a transition from classic to eco‐evolutionary cycles, and find evidence for eco‐evolutionary type cycles in about half of the studies. We show that rapid prey evolution is the most likely explanation for the observed patterns.     

Comparing disturbance and generalism in birds and mammals: A hump-shaped pattern

Using indices as proxies, we observed that comparing a large number of common birds and mammals, the level of generalism peaks in species inhabiting habitats at intermediate disturbance levels. This pattern might be universal, at least in these homeothermic vertebrates. Birds show nonetheless some differences in pattern from mammals, where specialization at intermediate levels of disturbance is not present. Differences in ecological and evolutionary traits between birds and mammals might determine different adaptive responses to historical anthropogenic changes, explaining these taxa-specific hump-shaped patterns.     

Origins of altruism diversity ii: runaway coevolution of altruistic strategies via "reciprocal niche construction"

Understanding the evolution of altruism requires knowledge of both its constraints and its drivers. Here we show that, paradoxically, ecological constraints on altruism may ultimately be its strongest driver. We construct a two-trait, coevolutionary adaptive dynamics model of social evolution in a genetically structured population with local resource competition. The intensity of local resource competition, which influences the direction and strength of social selection and which is typically treated as a static parameter, is here allowed to be an evolvable trait. Evolution of survival/fecundity altruism, which requires weak local competition, increases local competition as it evolves, creating negative environmental feedback that ultimately inhibits its further evolutionary advance. Alternatively, evolution of resource-based altruism, which requires strong local competition, weakens local competition as it evolves, also ultimately causing its own evolution to stall. When evolving independently, these altruistic strategies are intrinsically self-limiting. However, the coexistence of these two altruism types transforms the negative ecoevolutionary feedback generated by each strategy on itself into positive feedback on the other, allowing the presence of one trait to drive the evolution of the other. We call this feedback conversion "reciprocal niche construction." In the absence of constraints, this process leads to runaway coevolution of altruism types. We discuss applications to the origins and evolution of eusociality, division of labor, the inordinate ecological success of eusocial species, and the interaction between technology and demography in human evolution. Our theory suggests that the evolution of extreme sociality may often be an autocatalytic process.     

Eco-evolutionary consequences of habitat warming and fragmentation in communities

Eco-evolutionary dynamics can mediate species and community responses to habitat warming and fragmentation, two of the largest threats to biodiversity and ecosystems. The eco-evolutionary consequences of warming and fragmentation are typically studied independently, hindering our understanding of their simultaneous impacts. Here, we provide a new perspective rooted in trade-offs among traits for understanding their eco-evolutionary consequences. On the one hand, temperature influences traits related to metabolism, such as resource acquisition and activity levels. Such traits are also likely to have trade-offs with other energetically costly traits, like antipredator defences or dispersal. On the other hand, fragmentation can influence a variety of traits (e.g. dispersal) through its effects on the spatial environment experienced by individuals, as well as properties of populations, such as genetic structure. The combined effects of warming and fragmentation on communities should thus reflect their collective impact on traits of individuals and populations, as well as trade-offs at multiple trophic levels, leading to unexpected dynamics when effects are not additive and when evolutionary responses modulate them. Here, we provide a road map to navigate this complexity. First, we review single-species responses to warming and fragmentation. Second, we focus on consumer–resource interactions, considering how eco-evolutionary dynamics can arise in response to warming, fragmentation, and their interaction. Third, we illustrate our perspective with several example scenarios in which trait trade-offs could result in significant eco-evolutionary dynamics. Specifically, we consider the possible eco-evolutionary consequences of (i) evolution in thermal performance of a species involved in a consumer–resource interaction, (ii) ecological or evolutionary changes to encounter and attack rates of consumers, and (iii) changes to top consumer body size in tri-trophic food chains. In these scenarios, we present a number of novel, sometimes counter-intuitive, potential outcomes. Some of these expectations contrast with those solely based on ecological dynamics, for example, evolutionary responses in unexpected directions for resource species or unanticipated population declines in top consumers. Finally, we identify several unanswered questions about the conditions most likely to yield strong eco-evolutionary dynamics, how better to incorporate the role of trade-offs among traits, and the role of eco-evolutionary dynamics in governing responses to warming in fragmented communities.     

Intraspecific difference among herbivore lineages and their host‐plant specialization drive the strength of trophic cascades

Trophic cascades – the indirect effect of predators on non‐adjacent lower trophic levels – are important drivers of the structure and dynamics of ecological communities. However, the influence of intraspecific trait variation on the strength of trophic cascade remains largely unexplored, which limits our understanding of the mechanisms underlying ecological networks. Here we experimentally investigated how intraspecific difference among herbivore lineages specialized on different host plants influences trophic cascade strength in a terrestrial tri‐trophic system. We found that the occurrence and strength of the trophic cascade are strongly influenced by herbivores’ lineage and host‐plant specialization but are not associated with density‐dependent effects mediated by the growth rate of herbivore populations. Our findings stress the importance of intraspecific heterogeneities and evolutionary specialization as drivers of trophic cascade strength and underline that intraspecific variation should not be overlooked to decipher the joint influence of evolutionary and ecological factors on the functioning of multi‐trophic interactions.     

Joint evolution of specialization and dispersal in structured metapopulations

We study the joint evolution of dispersal and specialization concerning resource usage in a mechanistically underpinned structured discrete-time metapopulation model. We show that dispersal significantly affects the evolution of specialization and that specialization is a key factor that determines the possibility of evolutionary branching in dispersal propensity. Allowing both dispersal propensity and specialization to evolve as a consequence of natural selection is necessary in order to understand the evolutionary dynamics. The joint evolution of dispersal and specialization forms a natural evolutionary path leading to the coexistence of generalists and specialists. We show that in this process, the number of different patch types and the resource distribution are essential.     

Evolution of nutrient acquisition: when adaptation fills the gap between contrasting ecological theories

Although plant strategies for acquiring nutrients have been widely studied from a functional point of view, their evolution is still not well understood. In this study, we investigate the evolutionary dynamics of these strategies and determine how they influence ecosystem properties. To do so, we use a simple nutrient-limited ecosystem model in which plant ability to take up nutrients is subject to adaptive dynamics. We postulate the existence of a trade-off between this ability and mortality. We show that contrasting strategies are possible as evolutionary outcomes, depending on the shape of the trade-off and, when nitrogen is considered as the limiting nutrient, on the intensity of symbiotic fixation. Our model enables us to bridge these evolutionary outcomes to classical ecological theories such as Hardin''s tragedy of the commons and Tilman''s rule of R*. Evolution does not systematically maximize plant biomass or primary productivity. On the other hand, each evolutionary outcome leads to a decrease in the availability of the limiting mineral nutrient, supporting the work of Tilman on competition between plants for a single resource. Our model shows that evolution can be used to link different classical ecological results and that adaptation may influence ecosystem properties in contrasted ways.     

The adaptive dynamics of function-valued traits

This study extends the framework of adaptive dynamics to function-valued traits. Such adaptive traits naturally arise in a great variety of settings: variable or heterogeneous environments, age-structured populations, phenotypic plasticity, patterns of growth and form, resource gradients, and in many other areas of evolutionary ecology. Adaptive dynamics theory allows analysing the long-term evolution of such traits under the density-dependent and frequency-dependent selection pressures resulting from feedback between evolving populations and their ecological environment. Starting from individual-based considerations, we derive equations describing the expected dynamics of a function-valued trait in asexually reproducing populations under mutation-limited evolution, thus generalizing the canonical equation of adaptive dynamics to function-valued traits. We explain in detail how to account for various kinds of evolutionary constraints on the adaptive dynamics of function-valued traits. To illustrate the utility of our approach, we present applications to two specific examples that address, respectively, the evolution of metabolic investment strategies along resource gradients, and the evolution of seasonal flowering schedules in temporally varying environments.     

Effects of hummingbird morphology on specialization in pollination networks vary with resource availability

Specialization of species in interaction networks influences network stability and ecosystem functioning. Spatial and temporal variation in resource availability may provide insight into how ecological factors, such as resource abundance, and evolutionary factors, such as phylogenetically conserved morphological traits, influence specialization within mutualistic networks. We used independent measures of hummingbird abundance and resources (nectar), information on hummingbird traits and plant–hummingbird interactions to examine how resource availability and species' morphology influence the specialization of hummingbirds in three habitat types (forest, shrubs, cattle ranch) sampled over 10 sessions across two years in the southern Andes of Ecuador. Specialization of hummingbird species in the networks was measured by three indices: d' (related to niche partitioning), generality (related to niche width) and PSI (related to pollination services). Specialization indices d', generality and PSI of hummingbird species were influenced by resource availability. All indices indicated that specialization of hummingbirds increased when the availability of resources decreased. Variation in d' was also explained by an interaction between resource availability and bill length; hummingbirds with a long bill switched from being more specialized than other species when resource availability was low to being similarly specialized when availability was high. Overall, our results highlight the importance of ecological and evolutionary factors determining the specialization of species in interaction networks. We demonstrate in particular that ecological gradients in resource availability cause substantial changes in consumers' foraging behavior contingent on their morphology. Changes in pollinator specialization along resource gradients can have impacts on ecosystem functions, such as pollination by animals.     

The genetic architecture of ecological specialization: correlated gene effects on host use and habitat choice in pea aphids

Genetic correlations among phenotypic characters result when two traits are influenced by the same genes or sets of genes. By reducing the degree to which traits in two environments can evolve independently (e.g., Lande 1979; Via and Lande 1985), such correlations are likely to play a central role in both the evolution of ecological specialization and in its link to speciation. For example, negative genetic correlations between fitness traits in different environments (i.e., genetic trade-offs) are thought to influence the evolution of specialization, while positive genetic correlations between performance and characters influencing assortative mating can accelerate the evolution of reproductive isolation between ecologically specialized populations. We first discuss how the genetic architecture of a suite of traits may affect the evolutionary role of genetic correlations among them and review how the mechanisms of correlations can be analyzed using quantitative trait locus (QTL) mapping. We then consider the implications of such data for understanding the evolution of specialization and its link to speciation. We illustrate this approach with a QTL analysis of key characters in two races of pea aphids that are highly specialized on different host plants and partially reproductively isolated. Our results suggest that antagonism among QTL effects on performance in the two environments leads to a genetic trade-off in this system. We also found evidence for parallel QTL effects on host-plant acceptance and fecundity on the accepted host, which could produce assortative mating. These results suggest that the genetic architecture of traits associated with host use may have played a central role in the evolution of specialization and reproductive isolation in pea aphids.     

Parallelism in adaptive radiations of experimental Escherichia coli populations

Adaptive radiations are major contributors to species diversity. Although the underlying mechanisms of adaptive radiations, specialization and trade‐offs, are relatively well understood, the tempo and repeatability of adaptive radiations remain elusive. Ecological specialization can occur through the expansion into novel niches or through partitioning of an existing niche. To test how the mode of resource specialization affects the tempo and repeatability of adaptive radiations, we selected replicate bacterial populations in environments that promoted the evolution of diversity either through niche expansion or through niche partitioning, and in a third low‐quality single‐resource environment, in which diversity was not expected to evolve. Colony size diversity evolved equally fast in environments that provided ecological opportunities regardless of the mode of resource specialization. In the low‐quality environments, diversity did not consistently evolve. We observed the largest fitness improvement in the low‐quality environment and the smallest the glucose‐limited environment. We did not observe a change in the rate of evolutionary change in either trait or environment, suggesting that the pool of beneficial mutations was not exhausted. Overall, the mode of resource specialization did not affect the tempo or repeatability of adaptive radiations. These results demonstrate the limitations of eco‐evolutionary feedbacks to affect evolutionary outcomes.     

Cannibalism prevents evolutionary suicide of ontogenetic omnivores in life‐history intraguild predation systems

The majority of animal species are ontogenetic omnivores, that is, individuals of these species change or expand their diet during life. If small ontogenetic omnivores compete for a shared resource with their future prey, ecological persistence of ontogenetic omnivores can be hindered, although predation by large omnivores facilitates persistence. The coupling of developmental processes between different life stages might lead to a trade‐off between competition early in life and predation later in life, especially for ontogenetic omnivores that lack metamorphosis. By using bioenergetic modeling, we study how such an ontogenetic trade‐off affects ecological and evolutionary dynamics of ontogenetic omnivores. We find that selection toward increasing specialization of one life stage leads to evolutionary suicide of noncannibalistic ontogenetic omnivores, because it leads to a shift toward an alternative community state. Ontogenetic omnivores fail to re‐invade this new state due to the maladaptiveness of the other life stage. Cannibalism stabilizes selection on the ontogenetic trade‐off, prevents evolutionary suicide of ontogenetic omnivores, and promotes coexistence of omnivores with their prey. We outline how ecological and evolutionary persistence of ontogenetic omnivores depends on the type of diet change, cannibalism, and competitive hierarchy between omnivores and their prey.     

Origins of altruism diversity I: the diverse ecological roles of altruistic strategies and their evolutionary responses to local competition

Nature abounds with a rich variety of altruistic strategies, including public resource enhancement, resource provisioning, communal foraging, alarm calling, and nest defense. Yet, despite their vastly different ecological roles, current theory typically treats diverse altruistic traits as being favored under the same general conditions. Here, we introduce greater ecological realism into social evolution theory and find evidence of at least four distinct modes of altruism. Contrary to existing theory, we find that altruistic traits contributing to "resource-enhancement" (e.g., siderophore production, provisioning, agriculture) and "resource-efficiency" (e.g., pack hunting, communication) are most strongly favored when there is strong local competition. These resource-based modes of helping are "K-strategies" that increase a social group's growth yield, and should characterize species with scarce resources and/or high local crowding caused by low mortality, high fecundity, and/or mortality occurring late in the process of resource-acquisition. The opposite conditions, namely weak local competition (abundant resource, low crowding), favor survival (e.g., nest defense) and fecundity (e.g., nurse workers) altruism, which are "r-strategies" that increase a social group's growth rate. We find that survival altruism is uniquely favored by a novel evolutionary force that we call "sunk cost selection." Sunk cost selection favors helping that prevents resources from being wasted on individuals destined to die before reproduction. Our results contribute to explaining the observed natural diversity of altruistic strategies, reveal the necessary connection between the evolution and the ecology of sociality, and correct the widespread but inaccurate view that local competition uniformly impedes the evolution of altruism.     

Evolution of specialization and ecological character displacement of herbivores along a gradient of plant quality

We study the combined evolutionary dynamics of herbivore specialization and ecological character displacement, taking into account foraging behavior of the herbivores, and a quality gradient of plant types. Herbivores can adapt by changing two adaptive traits: their level of specialization in feeding efficiency and their point of maximum feeding efficiency along the plant gradient. The number of herbivore phenotypes, their levels of specialization, and the amount of character displacement among them are the result of the evolutionary dynamics, which is driven by the underlying population dynamics, which in turn is driven by the underlying foraging behavior. Our analysis demonstrates broad conditions for the diversification of a herbivore population into many specialized phenotypes, for basically any foraging behavior focusing use on highest gains while also including errors. Our model predicts two characteristic phases in the adaptation of herbivore phenotypes: a fast character-displacement phase and a slow coevolutionary niche-shift phase. This two-phase pattern is expected to be of wide relevance in various consumer-resource systems. Bringing together ecological character displacement and the evolution of specialization in a single model, our study suggests that the foraging behavior of herbivorous arthropods is a key factor promoting specialist radiation.     

Ecological specialization of mixotrophic plankton in a mixed water column

In recent years, the population dynamics of plankton in light- or nutrient-limited environments have been studied extensively. Their evolutionary dynamics, however, have received much less attention. Here, we used a modeling approach to study the evolutionary behavior of a population of plankton living in a mixed water column. Initially, the organisms are mixotrophic and thus have both autotrophic and heterotrophic abilities. Through evolution of their trophic preferences, however, they can specialize into separate autotrophs and heterotrophs. It was found that the light intensity gradient enables evolutionary branching and thus may result in the ecological specialization of the mixotrophs. By affecting the gradient, other environmental properties also acquire influence on this evolutionary process. Intermediate mixing intensities, large mixing depths, and high nutrient densities were found to facilitate evolutionary branching and thus specialization. Later results may explain why mixotrophs are often more dominant in oligotrophic systems while specialist strategies are associated with eutrophic systems.     

Ecological and evolutionary responses in complex communities: implications for invasions and eco‐evolutionary feedbacks

It is easier to predict the ecological and evolutionary outcomes of interactions in less diverse communities. As species are added to communities, their direct and indirect interactions multiply, their niches may shift, and there may be increased ecological redundancy. Accompanying this complexity in ecological interactions, is also complexity in selection and subsequent evolution, which may feed back to affect the ecology of the system, as species with different traits may play different ecological roles. Drawing from my own work and that of many others, I first discuss what we currently understand about ecology and evolution in light of simple and diverse communities, and suggest the importance of escape from community complexity per se in the success of invaders. Then, I examine how community complexity may influence the nature and magnitude of eco‐evolutionary feedbacks, classifying eco‐evolutionary dynamics into three general types: those generating alternative stable states, cyclic dynamics, and those maintaining ecological stasis and stability. The latter may be important and yet very hard to detect. I suggest future directions, as well as discuss methodological approaches and their potential pitfalls, in assessing the importance and longevity of eco‐evolutionary feedbacks in complex communities. Synthesis The ecology, evolution and eco‐evolutionary dynamics of simple and diverse communities are reviewed. In more diverse communities, direct and indirect interactions multiply, species’ niches often shift, ecological redundancy can increase, and selection may be less directional. Community complexity may influence the magnitude and nature of eco‐evolutionary dynamics, which are classified into three types: those generating alternative stable states, cyclic dynamics, and those maintaining ecological stasis and stability. Strengths and pitfalls of approaches to investigating eco‐evolutionary feedbacks in complex field communities are discussed.     

Local adaptation in dispersal in multi‐resource landscapes

The distribution of resources in space has important consequences for the evolution of dispersal‐related traits. Dispersal moderates patterns of gene flow and, consequently, the potential for local adaptation to spatially differentiated resource types. We lack both models and experiments that evaluate how dispersal evolves in landscapes with multiple resources. Here, we investigate the evolution of dispersal in landscapes that contain two resource types that differ in their spatial autocorrelations. Individuals may possess ecological traits that give them a fitness advantage on one or the other resource. We find that resources differing in their spatial autocorrelation select for different optimal dispersal strategies and, further, that some multi‐resource landscapes can support the stable coexistence of distinct dispersal strategies. Whether divergence in dispersal strategies between resource specialists occurs depends on the underlying structure of the resources and the degree of linkage between dispersal strategies and ecological specialization. This work indicates that the spatial autocorrelation of resources is an important factor in determining when evolutionary branching is likely to occur, and sheds light on when secondary isolating mechanisms should arise between locally adapted specialists.     

Pulsed-resource dynamics constrain the evolution of predator-prey interactions

Although temporal variability in the physical environment plays a major role in population fluctuations, little is known about how it drives the ecological and evolutionary dynamics of species interactions. We studied experimentally how extrinsic resource pulses affect evolutionary and ecological dynamics between the prey bacterium Serratia marcescens and the predatory protozoan Tetrahymena thermophila. Predation increased the frequency of defensive, nonpigmented prey types, which bore competitive costs in terms of reduced maximum growth rate, most in a constant-resource environment. Furthermore, the predator densities of the pulsed-resource environment regularly fluctuated above and below the mean predator densities of the constant environment. These results suggest that selection favored fast-growing competitor prey types over defensive but slower-growing prey types more often in the pulsed-resource environment (abundance of resources and low predation risk). As a result, the selection for prey defense fluctuated more in the pulsed-resource environment, leading to a weaker mean response in prey defense. At the ecological level, the evolution of prey defense weakened the relative strength of top-down regulation on prey community. This was more evident in the constant-resource environment, whereas the slow emergence of defensive prey types gradually decreased the amplitude of predator peaks in the pulsed-resource environment. Our study suggests that rapid evolution plays a smaller role in the ecological dynamics of communities dominated by resource pulses.