Sam P. Brown

Does multiple infection select for raised virulence

Classical models of virulence evolution conclude that the increased competition favoured by multiple infection will select for increasing consumption and deterioration of the host resource, or virulence. However, recent empirical and theoretical studies suggest that this view of virulence has some shortcomings. Here, we argue that the evolutionary consequences of multiple infection depend critically on whether the exploitation rate of an individual parasite is governed directly by the behaviour of the individual, or whether it is limited by the collective behaviour of the coinfecting group. We illustrate that, depending on the mechanistic details of exploitation, multiple infection can select for reduced virulence.

Understanding parasite strategies: a state-dependent approach?

Understanding and predicting parasite strategies is of interest not only for parasitologists, but also for anyone interested in epidemiology, control strategies and evolutionary medicine. From an ecological and evolutionary perspective, parasites are an important feature of their hosts selective environment, and may have diverse roles, ranging from the evolution of host sex to host-sexual selection behavior. Generally, it is the hosts and their biology that have been the focus of these evolutionary investigations, but we approach the subject from the parasites perspective, illustrating the sophistication of parasite strategies in dealing with contrasting and unpredictable environments.

An unlikely partnership: parasites, concomitant immunity and host defence

Concomitant immunity (CI) against macroparasites describes a state of effective anti–larval immunity coupled with persistent adult infection. Experimental studies indicate that immunologically concealed adult worms might promote anti–larval immunity via the release of cross–reactive antigens, thus creating a barrier against continual infection and restricting burden size within the host. CI offers an important potential benefit to established worms by preventing overcrowding within the host. Thus, CI may be interpreted as akin to vaccination; relatively long–lived adult worms ‘vaccinate’ their host with larval surface antigens and so benefit from reduced conspecific competition. The shared responsibility for host vaccination among adult worms leads to a problem of collective action. Here, we build on earlier analytical findings about the evolutionary forces that shape cooperation among parasites in order to produce a stochastic simulation model of macroparasite social evolution. First, we theoretically investigate a parasite adaptation hypothesis of CI and demonstrate its plausibility under defined conditions, despite the possibility of evolutionary ‘cheats’. Then we derive a set of predictions for testing the hypothesis that CI is partly a host–manipulative parasite adaptation. Evidence in support of this model would present an unusual case of adaptive population regulation.

The coevolution theory of autumn colours.

According to the coevolution theory of autumn colours, the bright colours of leaves in autumn are a warning signal to insects that lay their eggs on the trees in that season. If the colour is linked to the level of defensive commitment of the tree and the insects learn to avoid bright colours, this may lead to a coevolutionary process in which bright trees reduce their parasite load and choosy insects locate the most profitable hosts for the winter. We try to clarify what the theory actually says and to correct some misunderstandings that have been put forward. We also review current research on autumn colours and discuss what needs to be done to test the theory.

Evolution of trophic transmission in parasites: the need to reach a mating place?

Although numerous parasite species have a simple life cycle (SLC) and complete their life cycle in one host, there are other parasite species that exploit several host species successively. From an evolutionary perspective, understanding the mix of adaptive and contingent forces shaping the transition from an ancestral single‐host state to such a complex life cycle (CLC) has proved an intriguing challenge. In this paper, we propose a new hypothesis, which states that CLCs involving trophic transmission (i.e. transmission to a predator) evolved because they are an efficient way for parasites to meet a sexual partner, assuming that selective benefits are associated with cross‐fertilization. Predators that eat a lot of prey in a relatively short time interval act to concentrate isolated parasites. We use an optimality model to develop our hypothesis and discuss further directions of potential research.

SOCIALLY MEDIATED SPECIATION

Abstract We employ a simple model to show that social selection can lead to prezygotic reproductive isolation. The evolution of social discrimination causes the congealing of phenotypically similar individuals into different, spatially distinct tribes. However, tribal formation is only obtained for certain types of social behavior: altruistic and selfish acts can produce tribes, whereas spiteful and mutualistic behaviors never do. Moreover, reduced hybrid fitness at tribal borders leads to the selection of mating preferences, which then spread to the core areas of the respective tribes. Unlike models of resource competition, our model generates reproductive isolation in an ecologically homogeneous environment. We elaborate on how altruistic acts can lead to reproductive isolation, but also predict that certain types of competition can lead to the speciation effect. Our theory provides a framework for how individual-level interactions mold lineage diversification, with parapatric speciation as a possible end product.

Collective action in an RNA virus

A recent empirical study by Turner and Chao on the evolution of competitive interactions among phage virus strains revealed that a strain grown at high rates of co‐infection evolved towards lowered fitness relative to an ancestral strain. The authors went on to show that the fitness pay‐off matrix between the evolved and ancestral strain conforms to the prisoners’ dilemma. In this paper, I use Turner and Chao’s data to parameterize a simple model of parasite collective action. The prisoners’ dilemma is based on pairwise interactions of a discrete cooperate/defect nature. In contrast, the collective action model explicitly deals with individual–group interactions where the extent of cooperation is a continuous variable. I argue here that the ‘collective action’ modelling approach is more appropriate than the prisoners’ dilemma for the biology of virus evolution, and hence better able to form a predictive framework for further work on related strains of virus, linking mixing ecology, cooperative phenotype and fitness. Furthermore, the collective action model is used to motivate discussion on the evolutionary ecology of viruses, with a focus on the ‘levels of selection’ debate and the evolution of virulence.

Host manipulation by Ligula intestinalis : accident or adaptation?

Numerous studies have demonstrated that parasites with complex life-cycles can cause phenotypic modifications in their hosts that lead to an increased rate of transmission, and suggest that these modifications are the result of parasitic adaptations to manipulate the host. Little attention is paid, however, to separating the possibility of adaptive host manipulation from incidental (if fortuitous) side-effects of infection. In this study we combine statistical and analytical tools to interpret the impact of the macroparasite Ligula intestinalis L. (Cestoda, Pseudophyllidea) on the behaviour of its intermediate fish host (the roach, Rutilus rutilus L.), using field data on a natural system. Two distinct sets of generalized linear models agree that both the presence and the intensity of infection contribute to a modified behavioural response in the host. This was illustrated by a preference for the lake-edge in infected fish during autumn. Furthermore, the effect of parasites upon their host is heterogeneous with respect to parasite size, with larger parasite individuals having a disproportionate impact. A series of game-theoretic models of adaptive host manipulation illustrate a potential rationale for a size-dependent manipulation strategy in parasites. These findings illustrate the potential complexity and functionality of the impact of L. intestinalis upon its fish host, which together reduce the parsimony of the alternative incidental effect hypothesis.

Defence against multiple enemies

Although very common under natural conditions, the consequences of multiple enemies (parasites, predators, herbivores, or even ‘chemical’ enemies like insecticides) on investment in defence has scarcely been investigated. In this paper, we present a simple model of the joint evolution of two defences targeted against two enemies. We illustrate how the respective level of each defence can be influenced by the presence of the two enemies. Furthermore, we investigate the influences of direct interference and synergy between defences. We show that, depending on certain conditions (costs, interference or synergy between defences), an increase in selection pressure by one enemy can have dramatic effects on defence against another enemy. It is generally admitted that increasing the encounter rate with a second natural enemy can decrease investment in defence against a first enemy, but our results indicate that it may sometimes favour resistance against the first enemy. Moreover, we illustrate that the global defence against one enemy can be lower when only this enemy is present: this has important implications for experimental measures of resistance, and for organisms that invade an area with less enemies or whose community of enemies is reduced. We discuss possible implications of the existence of multiple enemies for conservation biology, biological control and chemical control.

Human birthweight evolution across contrasting environments

We explore from both theoretical and empirical perspectives the hypothesis that a significant part of the worldwide variability in human birthweight results from adaptive responses to local selective pressures. We first developed an agent‐based model to simulate the process of evolutionary selection on life history strategy, and then we performed a comparative analysis across 89 countries worldwide. The model illustrates that optimal birthweight depends on which fitness‐reducing risk locally predominates (somatic diseases, parasitic diseases or adverse environmental conditions). When fitness variations between individuals mainly result from somatic diseases (e.g. industrialized countries), or conversely from infectious and parasitic diseases (e.g. developing countries), selection is expected to favour individuals producing larger children. Conversely, when environmental risks increase in relative importance, selective pressures for producing children with high birthweight are reduced. The comparative analysis supports these theoretical expectations, in particular the finding that birthweight is higher than predicted in highly parasitized countries.