Evolution of cannibalistic traits: scenarios derived from adaptive dynamics

The evolution of cannibalistic traits in consumer populations is studied in this paper with the approach of adaptive dynamics theory. The model is kept at its minimum complexity by eliminating some environmental characteristics, like heterogeneity and seasonalities, and by hiding the size-structure of the population. Evolutionary dynamics are identified through numerical bifurcation analysis, applied both to the ecological (resident-mutant) model and to the canonical equation of adaptive dynamics. The result is a rich catalog of evolutionary scenarios involving evolutionary stable strategies and branching points both in the monomorphic and dimorphic dynamics. The possibility of evolutionary extinction of highly cannibalistic populations is also ascertained. This allows one to explain why cannibalism can be a transient stage of evolution.     

Remarks on branching-extinction evolutionary cycles

We show in this paper that the evolution of cannibalistic consumer populations can be a never ending story involving alternating levels of polymorphism. More precisely, we show that a monomorphic population can evolve toward high levels of cannibalism until it reaches a so-called branching point, where the population splits into two sub-populations characterized by different, but initially very close, cannibalistic traits. Then, the two traits coevolve until the more cannibalistic sub-population undergoes evolutionary extinction. Finally, the remaining population evolves back to the branching point, thus closing an evolutionary cycle. The model on which the study is based is purely deterministic and derived through the adaptive dynamics approach. Evolutionary dynamics are investigated through numerical bifurcation analysis, applied both to the ecological (resident-mutant) model and to the evolutionary model. The general conclusion emerging from this study is that branching-extinction evolutionary cycles can be present in wide ranges of environmental and demographic parameters, so that their detection is of crucial importance when studying evolutionary dynamics.     

Evolutionary potential of a widespread clonal grass under changing climate

Adaptive responses are probably the most effective long‐term responses of populations to climate change, but they require sufficient evolutionary potential upon which selection can act. This requires high genetic variance for the traits under selection and low antagonizing genetic covariances between the different traits. Evolutionary potential estimates are still scarce for long‐lived, clonal plants, although these species are predicted to dominate the landscape with climate change. We studied the evolutionary potential of a perennial grass, Festuca rubra, in western Norway, in two controlled environments corresponding to extreme environments in natural populations: cold–dry and warm–wet, the latter being consistent with the climatic predictions for the country. We estimated genetic variances, covariances, selection gradients and response to selection for a wide range of growth, resource acquisition and physiological traits, and compared their estimates between the environments. We showed that the evolutionary potential of F. rubra is high in both environments, and genetic covariances define one main direction along which selection can act with relatively few constraints to selection. The observed response to selection at present is not sufficient to produce genotypes adapted to the predicted climate change under a simple, space for time substitution model. However, the current populations contain genotypes which are pre‐adapted to the new climate, especially for growth and resource acquisition traits. Overall, these results suggest that the present populations of the long‐lived clonal plant may have sufficient evolutionary potential to withstand long‐term climate changes through adaptive responses.     

Function-valued adaptive dynamics and the calculus of variations

Adaptive dynamics has been widely used to study the evolution of scalar-valued, and occasionally vector-valued, strategies in ecologically realistic models. In many ecological situations, however, evolving strategies are best described as function-valued, and thus infinite-dimensional, traits. So far, such evolution has only been studied sporadically, mostly based on quantitative genetics models with limited ecological realism. In this article we show how to apply the calculus of variations to find evolutionarily singular strategies of function-valued adaptive dynamics: such a strategy has to satisfy Euler's equation with environmental feedback. We also demonstrate how second-order derivatives can be used to investigate whether or not a function-valued singular strategy is evolutionarily stable. We illustrate our approach by presenting several worked examples.     

Biogeography of species richness gradients: linking adaptive traits,demography and diversification

Here we review how adaptive traits contribute to the emergence and maintenance of species richness gradients through their influence on demographic and diversification processes. We start by reviewing how demographic dynamics change along species richness gradients. Empirical studies show that geographical clines in population parameters and measures of demographic variability are frequent along latitudinal and altitudinal gradients. Demographic variability often increases at the extremes of regional species richness gradients and contributes to shape these gradients. Available studies suggest that adaptive traits significantly influence demographic dynamics, and set the limits of species distributions. Traits related to thermal tolerance, resource use, phenology and dispersal seem to play a significant role. For many traits affecting demography and/or diversification processes, complex mechanistic approaches linking genotype, phenotype and fitness are becoming progressively available. In several taxa, species can be distributed along adaptive trait continuums, i.e. a main axis accounting for the bulk of inter‐specific variation in some correlated adaptive traits. It is shown that adaptive trait continuums can provide useful mechanistic frameworks to explain demographic dynamics and diversification in species richness gradients. Finally, we review the existence of sequences of adaptive traits in phylogenies, the interactions of adaptive traits and community context, the clinal variation of traits across geographical gradients, and the role of adaptive traits in determining the history of dispersal and diversification of clades. Overall, we show that the study of demographic and evolutionary mechanisms that shape species richness gradients clearly requires the explicit consideration of adaptive traits. To conclude, future research lines and trends in the field are briefly outlined.     

How phenotypic convergence arises in experimental evolution

Evolutionary convergence is a core issue in the study of adaptive evolution, as well as a highly debated topic at present. Few studies have analyzed this issue using a “real‐time” or evolutionary trajectory approach. Do populations that are initially differentiated converge to a similar adaptive state when experiencing a common novel environment? Drosophila subobscura populations founded from different locations and years showed initial differences and variation in evolutionary rates in several traits during short‐term (～20 generations) laboratory adaptation. Here, we extend that analysis to 40 more generations to analyze (1) how differences in evolutionary dynamics among populations change between shorter and longer time spans, and (2) whether evolutionary convergence occurs after 60 generations of evolution in a common environment. We found substantial variation in longer term evolutionary trajectories and differences between short‐ and longer term evolutionary dynamics. Although we observed pervasive patterns of convergence toward the character values of long‐established populations, populations still remain differentiated for several traits at the final generations analyzed. This pattern might involve transient divergence, as we report in some cases, indicating that more generations should lead to final convergence. These findings highlight the importance of longer term studies for understanding convergent evolution.     

Variant evolutionary trees under phenotypic variance

Evolutionary branching, which is a coevolutionary phenomenon of the development of two or more distinctive traits from a single trait in a population, is the issue of recent studies on adaptive dynamics. In previous studies, it was revealed that trait variance is a minimum requirement for evolutionary branching, and that it does not play an important role in the formation of an evolutionary pattern of branching. Here we demonstrate that the trait evolution exhibits various evolutionary branching paths starting from an identical initial trait to different evolutional terminus traits as determined by only changing the assumption of trait variance. The key feature of this phenomenon is the topological configuration of equilibria and the initial point in the manifold of dimorphism from which dimorphic branches develop. This suggests that the existing monomorphic or polymorphic set in a population is not an unique inevitable consequence of an identical initial phenotype.     

Cast adrift on an island: introduced populations experience an altered balance between selection and drift

A long-standing question in evolutionary biology is what becomes of adaptive traits when a species expands its range into novel environments. Here, we report the results of a study on an adaptive colour pattern polymorphism (stripes) of the coqui frog, Eleutherodactylus coqui, following its introduction to Hawaii from Puerto Rico. We compared population differentiation ( ) for the stripes locus-which underlies this colour pattern polymorphism-with neutral microsatellite loci to test for a signature of selection among native and introduced populations. Among native populations, for stripes were lower than expected under the neutral model, suggesting uniform balancing selection. Alternatively, among introduced populations, for stripes did not differ from the neutral model. These results suggest that the evolutionary dynamics of this previously adaptive trait have become dominated by random genetic drift following the range expansion.     

Variation,selection and evolution of function-valued traits

We describe an emerging framework for understanding variation, selection and evolution of phenotypic traits that are mathematical functions. We use one specific empirical example – thermal performance curves (TPCs) for growth rates of caterpillars – to demonstrate how models for function-valued traits are natural extensions of more familiar, multivariate models for correlated, quantitative traits. We emphasize three main points. First, because function-valued traits are continuous functions, there are important constraints on their patterns of variation that are not captured by multivariate models. Phenotypic and genetic variation in function-valued traits can be quantified in terms of variance-covariance functions and their associated eigenfunctions: we illustrate how these are estimated as well as their biological interpretations for TPCs. Second, selection on a function-valued trait is itself a function, defined in terms of selection gradient functions. For TPCs, the selection gradient describes how the relationship between an organism's performance and its fitness varies as a function of its temperature. We show how the form of the selection gradient function for TPCs relates to the frequency distribution of environmental states (caterpillar temperatures) during selection. Third, we can predict evolutionary responses of function-valued traits in terms of the genetic variance-covariance and the selection gradient functions. We illustrate how non-linear evolutionary responses of TPCs may occur even when the mean phenotype and the selection gradient are themselves linear functions of temperature. Finally, we discuss some of the methodological and empirical challenges for future studies of the evolution of function-valued traits.     

Availability of prey resources drives evolution of predator-prey interaction

Productivity is predicted to drive the ecological and evolutionary dynamics of predator-prey interaction through changes in resource allocation between different traits. Here we report results of an evolutionary experiment where prey bacteria Serratia marcescens was exposed to predatory protozoa Tetrahymena thermophila in low- and high-resource environments for approximately 2400 prey generations. Predation generally increased prey allocation to defence and caused prey selection lines to become more diverse. On average, prey became most defensive in the high-resource environment and suffered from reduced resource use ability more in the low-resource environment. As a result, the evolution of stronger prey defence in the high-resource environment led to a strong decrease in predator-to-prey ratio. Predation increased temporal variability of populations and traits of prey. However, this destabilizing effect was less pronounced in the high-resource environment. Our results demonstrate that prey resource availability can shape the trade-off allocation of prey traits, which in turn affects multiple properties of the evolving predator-prey system.     

The evolution of function-valued traits for conditional cooperation

In this paper we study the evolution of function-valued traits for cooperation in environments that display varying degrees of population viscosity. Traits measure an individual's intrinsic propensity to cooperate in a standard bilateral Prisoner's dilemma and can be increasing, decreasing or constant functions of the probability to interact with individuals of ones own genotype. We first analyse adaptation to homogenous environments (with constant degree of viscosity). Comparing environments characterized by different degrees of viscosity, we find that the relation between viscosity and the equilibrium type distribution is not monotone. In fact, it is possible that in fluid populations (no viscosity) there is more cooperation in equilibrium than in populations with intermediate degrees of viscosity. In a second step we analyse heterogenous environments (with varying degrees of viscosity). We find that under very weak assumptions on the distribution of the viscosity parameter strictly increasing functions are always selected and under some parameter constellations they are uniquely so.     

A model for the evolutionary dynamics of cross-feeding polymorphisms in microorganisms

 Understanding mechanisms of evolutionary diversification is central to evolutionary biology. Microbes constitute promising model systems for observing processes of diversification directly in the laboratory. One of the main existing paradigms for microbial diversification is the evolution of cross-feeding polymorphisms, in which a strain specializing on a primary resource coexists with a cross-feeding strain that specializes on a waste product resulting from consumption of the primary resource. Here I propose a theoretical model for the evolutionary dynamics through which cross-feeding polymorphisms can gradually emerge from a single ancestral strain. The model is based on the framework of adaptive dynamics, which has proved to be very useful for studying adaptive processes of divergence under sympatric conditions. In particular, the phenomenon of evolutionary branching serves as a general paradigm for diversification. I show that evolutionary branching naturally occurs in evolutionary models of cross-feeding if (1) there is a trade-off between uptake efficiencies on the primary and secondary resources, and (2) this trade-off has positive curvature. The model also suggests that the evolution of cross-feeding should be more likely in chemostat cultures than in serial batch cultures, which conforms with empirical observations. Overall, the model provides a theoretical metaphor for the evolution of cross-feeding polymorphisms. Received: February 19, 2002 / Accepted: May 8, 2002     

Multiple Novel Traits without Immediate Benefits Originate in Bacteria Evolving on Single Antibiotics

How new traits originate in evolution is a fundamental question of evolutionary biology. When such traits arise, they can either be immediately beneficial in their environment of origin, or they may become beneficial only in a future environment. Compared to immediately beneficial novel traits, novel traits without immediate benefits remain poorly studied. Here we use experimental evolution to study novel traits that are not immediately beneficial but that allow bacteria to survive in new environments. Specifically, we evolved multiple E. coli populations in five antibiotics with different mechanisms of action, and then determined their ability to grow in more than 200 environments that are different from the environment in which they evolved. Our populations evolved viability in multiple environments that contain not just clinically relevant antibiotics, but a broad range of antimicrobial molecules, such as surfactants, organic and inorganic salts, nucleotide analogues and pyridine derivatives. Genome sequencing of multiple evolved clones shows that pleiotropic mutations are important for the origin of these novel traits. Our experiments, which lasted fewer than 250 generations, demonstrate that evolution can readily create an enormous reservoir of latent traits in microbial populations. These traits can facilitate adaptive evolution in a changing world.     

Adaptive evolution of foraging-related traits in a predator-prey community

In this paper, with the method of adaptive dynamics and geometric technique, we investigate the adaptive evolution of foraging-related phenotypic traits in a predator-prey community with trade-off structure. Specialization on one prey type is assumed to go at the expense of specialization on another. First, we identify the ecological and evolutionary conditions that allow for evolutionary branching in predator phenotype. Generally, if there is a small switching cost near the singular strategy, then this singular strategy is an evolutionary branching point, in which predator population will change from monomorphism to dimorphism. Second, we find that if the trade-off curve is globally convex, predator population eventually branches into two extreme specialists, each completely specializing on a particular prey species. However, if the trade-off curve is concave-convex-concave, after branching in predator phenotype, the two predator species will evolve to an evolutionarily stable dimorphism at which they can continue to coexist. The analysis reveals that an attractive dimorphism will always be evolutionarily stable and that no further branching is possible under this model.     

Study of Natural Genetic Variation in Early Fitness Traits Reveals Decoupling Between Larval and Pupal Developmental Time in <Emphasis Type="Italic">Drosophila melanogaster</Emphasis>

Characterizing the relationships between genotype and phenotype for developmental adaptive traits is essential to understand the evolutionary dynamics underlying biodiversity. In holometabolous insects, the time to reach the reproductive stage and pupation site preference are two such traits. Here we characterize aspects of the genetic architecture for Developmental Time (decomposed in Larval and Pupal components) and Pupation Height using lines derived from three natural populations of Drosophila melanogaster raised at two temperatures. For all traits, phenotypic differences and variation in plasticity between populations suggest adaptation to the original thermal regimes. However, high variability within populations shows that selection does not exhaust genetic variance for these traits. This could be partly explained by local adaptation, environmental heterogeneity and modifications in the genetic architecture of traits according to environment and ontogenetic stage. Indeed, our results show that the genetic factors affecting Developmental Time and Pupation Height are temperature-specific. Varying relationships between Larval and Pupal Developmental Time between and within populations also suggest stage-specific modifications of genetic architecture for this trait. This flexibility would allow for a somewhat independent evolution of adaptive traits at different environments and life stages, favoring the maintenance of genetic variability and thus sustaining the traits’ evolvabilities.     

Constraints on the evolution of adaptive plasticity: costs of plasticity to density are expressed in segregating progenies

Phenotypic plasticity, the ability of a genotype to express different phenotypes across environments, is an adaptive strategy expected to evolve in heterogeneous environments. One widely held hypothesis is that the evolutionary benefits of plasticity are reduced by its costs, but when compared with the number of traits tested, the evidence for costs is limited. Selection gradients were calculated for traits and trait plasticities to test for costs of plasticity to density in a field study using recombinant inbred lines (RILs) of Brassica rapa. Significant costs of putatively adaptive plasticity were found in three out of six measured traits. For one trait, petiole length, a cost of plasticity was detected in both environments tested; such global costs are expected to more strongly constrain the evolution of plasticity than local costs expressed in a single environment. These results, in combination with evidence from studies in segregating progenies of Arabidopsis thaliana, suggest that the potential for genetic costs of plasticity exists in natural populations. Detection of costs in previous studies may have been limited because historical selection has purged genotypes with costly plasticity, and experimental conditions often lack environmental stresses.     

THE RESPONSE TO DIFFERING SELECTION ON PLANT PHYSIOLOGICAL TRAITS: EVIDENCE FOR LOCAL ADAPTATION

Understanding adaptive evolution to differing environments requires studies of genetic variances, of natural selection, and of the genetic differentiation between populations. Plant physiological traits such as leaf size and water-use efficiency (the ratio of carbon gained per water lost) have been suggested by physiological plant ecologists to be important in local adaptation to environments differing in water availability. In this study, I raised families of Cakile edentula var lacustris derived from a wet-site population and a dry-site population in a common greenhouse environment to determine the degree of genetic differentiation between the two populations and the genetic architecture of the traits. The dry-site population had significantly smaller leaf size and significantly greater water-use efficiency than the wet-site population. I used a retrospective selection analysis to compare long-term selection inferred from these results to measures of phenotypic selection from a field experiment. Both direct measures in the field and the retrospective selection gradients were consistent with the hypothesis that greater water-use efficiency and smaller leaves were adaptive in drier environments. Though the correlation between population means for water-use efficiency and leaf size was negative, the genetic correlation within populations between water-use efficiency and leaf size was positive and thus would be expected to constrain the evolutionary response to selection.     

Environment-dependent inbreeding depression: its ecological and evolutionary significance

Inbreeding depression is a major evolutionary and ecological force that influences population dynamics and the evolution of inbreeding-avoidance traits such as mating systems and dispersal. There is now compelling evidence that inbreeding depression is environment-dependent. Here, we discuss ecological and evolutionary consequences of environment-dependent inbreeding depression. The environmental dependence of inbreeding depression may be caused by environment-dependent phenotypic expression, environment-dependent dominance, and environment-dependent natural selection. The existence of environment-dependent inbreeding depression challenges classical models of inbreeding as caused by unconditionally deleterious alleles, and suggests that balancing selection may shape inbreeding depression in natural populations; loci associated with inbreeding depression in some environments may even contribute to adaptation to others. Environment-dependent inbreeding depression also has important, often neglected, ecological and evolutionary consequences: it can influence the demography of marginal or colonizing populations and alter adaptive optima of mating systems, dispersal, and their associated traits. Incorporating the environmental dependence of inbreeding depression into theoretical models and empirical studies is necessary for understanding the genetic and ecological basis of inbreeding depression and its consequences in natural populations.     

Adaptive and non‐adaptive evolution of trait means and genetic trait correlations for herbivory resistance and performance in an invasive plant

The EICA‐hypothesis predicts that invading plants adapt to their novel environment by evolving increased performance and reduced resistance in response to the release from natural enemies, and assumes a resource allocation tradeoff among both trait groups as mechanistic basis of this evolutionary change. Using the plant Silene latifolia as a study system, we tested these predictions by investigating whether 1) invasive populations evolved lower resistance and higher performance, 2) this evolutionary change is indeed adaptive, and 3) there is a negative genetic correlation between performance and resistance (i.e. a tradeoff) in native and introduced individuals. Moreover, we sampled eight native and eight invasive populations and determined their population co‐ancestry based on neutral SSR‐markers. We performed controlled crossings to produce five sib‐groups per population and exposed them to increased and reduced levels of enemy attack in a full‐factorial experiment to estimate performance and resistance. With these data, we performed trait‐by‐trait comparisons between ranges with ‘animal models’ that account for population co‐ancestry to quantify the amount of variance in traits explained by non‐adaptive versus adaptive evolution. Moreover, we tested for genetic correlations among performance and resistance traits within sib‐groups. We found significant reductions in resistance and increases in performance in invasive versus native populations, which could largely be attributed to adaptive evolution. While we detected a non‐significant trend towards negative genetic performance × resistance correlations in native populations, invasive populations exhibited both significant and non‐significant positive correlations. In summary, these results do not support a shift of performance and resistance trait values along a tradeoff line in response to enemy release, as predicted by EICA. They rather suggest that the independent evolution of both traits is not constrained by a tradeoff, and that various selective agents (including resource availability) interact in shaping both traits and in weakening negative genetic correlations in the invaded habitat.