Martijn Egas

The economics of altruistic punishment and the maintenance of cooperation

Explaining the evolution and maintenance of cooperation among unrelated individuals is one of the fundamental problems in biology and the social sciences. Recent findings suggest that altruistic punishment is an important mechanism maintaining cooperation among humans. We experimentally explore the boundaries of altruistic punishment to maintain cooperation by varying both the cost and the impact of punishment, using an exceptionally extensive subject pool. Our results show that cooperation is only maintained if conditions for altruistic punishment are relatively favourable: low cost for the punisher and high impact on the punished. Our results indicate that punishment is strongly governed by its cost-to-impact ratio and that its effect on cooperation can be pinned down to one single variable: the threshold level of free-riding that goes unpunished. Additionally, actual pay-offs are the lowest when altruistic punishment maintains cooperation, because the pay-off destroyed through punishment exceeds the gains from increased cooperation. Our results are consistent with the interpretation that punishment decisions come from an amalgam of emotional response and cognitive cost–impact analysis and suggest that altruistic punishment alone can hardly maintain cooperation under multi-level natural selection. Uncovering the workings of altruistic punishment as has been done here is important because it helps predicting under which conditions altruistic punishment is expected to maintain cooperation.

Evolution restricts the coexistence of specialists and generalists: the role of trade-off structure

Environmental variability and adaptive foraging behavior have been shown to favor coexistence of specialists and generalists on an ecological timescale. This leaves unaddressed the question of whether such coexistence can also be expected on an evolutionary timescale. In this article, we study the attainability, through gradual evolution, of specialist‐generalist coexistence, as well as the evolutionary stability of such communities when allowing for immigration. Our analysis shows that the potential for specialist‐generalist coexistence is much more restricted than originally thought and strongly depends on the trade‐off structure assumed. We establish that ecological coexistence is less likely for species facing a trade‐off between per capita reproduction in different habitats than when the trade‐off acts on carrying capacities alone. We also demonstrate that coexistence is evolutionarily stable whenever it is ecologically stable but that in most cases, such coexistence cannot be reached through gradual evolution. We conclude that an evolutionarily stable community of specialists and generalists may be created only through immigration from elsewhere or through mutations of large effect. Our results highlight that trade‐offs in fitness‐determining traits can have counterintuitive effects on the evolution of specialization.

Wolbachia affects oviposition and mating behaviour of its spider mite host

Wolbachia bacteria are transmitted from mother to offspring via the cytoplasm of the egg. When mated to males infected with Wolbachia bacteria, uninfected females produce unviable offspring, a phenomenon called cytoplasmic incompatibility (CI). Current theory predicts that ‘sterilization’ of uninfected females by infected males confers a fitness advantage to Wolbachia in infected females. When the infection is above a threshold frequency in a panmictic population, CI reduces the fitness of uninfected females below that of infected females and, consequently, the proportion of infected hosts increases. CI is a mechanism that benefits the bacteria but, apparently, not the host. The host could benefit from avoiding incompatible mates. Parasite load and disease resistance are known to be involved in mate choice. Can Wolbachia also be implicated in reproductive behaviour? We used the two‐spotted spider mite – Wolbachia symbiosis to address this question. Our results suggest that uninfected females preferably mate to uninfected males while infected females aggregate their offspring, thereby promoting sib mating. Our data agrees with other results that hosts of Wolbachia do not necessarily behave as innocent bystanders – host mechanisms that avoid CI can evolve.

The Timescale of Phenotypic Plasticity and Its Impact on Competition in Fluctuating Environments

Although phenotypic plasticity can be advantageous in fluctuating environments, it may come too late if the environment changes fast. Complementary chromatic adaptation is a colorful form of phenotypic plasticity, where cyanobacteria tune their pigmentation to the prevailing light spectrum. Here, we study the timescale of chromatic adaptation and its impact on competition among phytoplankton species exposed to fluctuating light colors. We parameterized a resource competition model using monoculture experiments with green and red picocyanobacteria and the cyanobacterium Pseudanabaena, which can change its color within ∼7 days by chromatic adaptation. The model predictions were tested in competition experiments, where the incident light color switched between red and green at different frequencies (slow, intermediate, and fast). Pseudanabaena (the flexible phenotype) competitively excluded the green and red picocyanobacteria in all competition experiments. Strikingly, the rate of competitive exclusion was much faster when the flexible phenotype had sufficient time to fully adjust its pigmentation. Thus, the flexible phenotype benefited from its phenotypic plasticity if fluctuations in light color were relatively slow, corresponding to slow mixing processes or infrequent storms in their natural habitat. This shows that the timescale of phenotypic plasticity plays a key role during species interactions in fluctuating environments.

Are adaptation costs necessary to build up a local adaptation pattern

BackgroundEcological specialization is pervasive in phytophagous arthropods. In such specialization mode, limits to host range are imposed by trade-offs preventing adaptation to several hosts. The occurrence of such trade-offs is inferred by a pattern of local adaptation, i.e., a negative correlation between relative performance on different hosts.ResultsTo establish a causal link between local adaptation and trade-offs, we performed experimental evolution of spider mites on cucumber, tomato and pepper, starting from a population adapted to cucumber. Spider mites adapted to each novel host within 15 generations and no further evolution was observed at generation 25. A pattern of local adaptation was found, as lines evolving on a novel host performed better on that host than lines evolving on other hosts. However, costs of adaptation were absent. Indeed, lines adapted to tomato had similar or higher performance on pepper than lines evolving on the ancestral host (which represent the initial performance of all lines) and the converse was also true, e.g. negatively correlated responses were not observed on the alternative novel host. Moreover, adapting to novel hosts did not result in decreased performance on the ancestral host. Adaptation did not modify host ranking, as all lines performed best on the ancestral host. Furthermore, mites from all lines preferred the ancestral to novel hosts. Mate choice experiments indicated that crosses between individuals from the same or from a different selection regime were equally likely, hence development of reproductive isolation among lines adapted to different hosts is unlikely.ConclusionTherefore, performance and preference are not expected to impose limits to host range in our study species. Our results show that the evolution of a local adaptation pattern is not necessarily associated with the evolution of an adaptation cost.

Evolution of Specialization and Ecological Character Displacement of Herbivores along a Gradient of Plant Quality

Abstract 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 consumerresource 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.

On the evolution of cytoplasmic incompatibility in haplodiploid species.

Abstract The most enigmatic sexual manipulation by Wolbachia endosymbionts is cytoplasmic incompatibility (CI): infected males are reproductively incompatible with uninfected females. In this paper, we extend the theory on population dynamics and evolution of CI, with emphasis on haplodiploid species. First, we focus on the problem of the threshold to invasion of the Wolbachia infection in a population. Simulations of the dynamics of infection in small populations show that it does not suffice to assume invasion by drift alone (or demographic “accident”). We propose several promising alternatives that may facilitate invasion of Wolbachia in uninfected populations: sex‐ratio effects, meta population structure, and other fitness‐compensating effects. Including sex‐ratio effects of Wolbachia allows invasion whenever infected females produce more infected daughters than uninfected females produce uninfected daughters. Several studies on haplodiploid species suggest the presence of such sex‐ratio effects. The simple meta‐population model we analyzed predicts that, given that infecteds are better “invaders”, uninfecteds must be better “colonizers” to maintain coexistence of infected and uninfected patches. This condition seems more feasible for species that suffer local extinction due to predation (or parasitization) than for species that suffer local extinction due to overexploiting their resource(s). Finally, we analyze the evolution of CI in haplodiploids once a population has been infected. Evolution does not depend on the type of CI (female mortality or male production), but hinges solely on decreasing the fitness cost and/or increasing the transmission efficiency. Our models offer new perspectives for increasing our understanding of the population and evolutionary dynamics of CI.

Evolutionary Predictions Should Be Based on Individual-Level Traits

Recent theoretical studies have analyzed the evolution of habitat specialization using either the logistic or the Ricker equation. These studies have implemented evolutionary change directly in population‐level parameters such as habitat‐specific intrinsic growth rates r or carrying capacities K. This approach is a shortcut to a more detailed analysis where evolutionary change is studied in underlying morphological, physiological, or behavioral traits at the level of the individual that contribute to r or K. Here we describe two pitfalls that can occur when such a shortcut is employed. First, population‐level parameters that appear as independent variables in a population dynamical model might not be independent when derived from processes at the individual level. Second, patterns of covariation between individual‐level traits are usually not conserved when mapped to the level of demographic parameters. Nonlinear mappings constrain the curvature of trade‐offs that can sensibly be assumed at the population level. To illustrate these results, we derive a two‐habitat version of the logistic and Ricker equations from individual‐level processes and compare the evolutionary dynamics of habitat‐specific carrying capacities with those of underlying individual‐level traits contributing to the carrying capacities. Finally, we sketch how our viewpoint affects the results of earlier studies.

How Adaptive Learning Affects Evolution: Reviewing Theory on the Baldwin Effect.

We review models of the Baldwin effect, i.e., the hypothesis that adaptive learning (i.e., learning to improve fitness) accelerates genetic evolution of the phenotype. Numerous theoretical studies scrutinized the hypothesis that a non-evolving ability of adaptive learning accelerates evolution of genetically determined behavior. However, their results are conflicting in that some studies predict an accelerating effect of learning on evolution, whereas others show a decelerating effect. We begin by describing the arguments underlying the hypothesis on the Baldwin effect and identify the core argument: adaptive learning influences the rate of evolution because it changes relative fitness of phenotypes. Then we analyze the theoretical studies of the Baldwin effect with respect to their model of adaptive learning and discuss how their contrasting results can be explained from differences in (1) the ways in which the effect of adaptive learning on the phenotype is modeled, (2) the assumptions underlying the function used to quantify fitness and (3) the time scale at which the evolutionary rate is measured. We finish by reviewing the specific assumptions used by the theoretical studies of the Baldwin effect and discuss the evolutionary implications for cases where these assumptions do not hold.

Pheromone-Induced Priming of a Defensive Response in Western Flower Thrips

The Western flower thrips Frankliniella occidentalis produces conspicuous anal droplets that function as a direct defense against various predators. These droplets also function in pheromonal communication in that they contain a mixture of decyl acetate and dodecyl acetate, which acts as an alarm. Exposure of thrips to synthetic pheromone is known to promote takeoff or refuge seeking, but the effect of the natural pheromone has not yet been studied. Here, we not only studied the response to natural pheromone, but also tested the new hypothesis that the alarm pheromone primes a defensive response in thrips. This test was carried out by measuring the reaction time to a simulated predator attack after exposure to synthetic or natural alarm pheromone (against a control with no pheromone at all). The reaction was quantified in terms of the time it takes a thrips larva to produce a droplet after attack. We found that thrips larvae produce droplets of alarm pheromone faster when cues associated with danger are present. There were no significant differences in reaction times of responses to synthetic pheromone, natural pheromone, or odors from a patch with a predator attacking a thrips larva. This implies that the synthetic pheromone mimics the natural pheromone, and that other cues emanating from the predator play a minor role. We conclude that the alarm pheromone increases the vigilance of the thrips, and this may promote its survival.