The evolution of resistance through costly acquired immunity

We examine the evolutionary dynamics of resistance to parasites through acquired immunity. Resistance can be achieved through the innate mechanisms of avoidance of infection and reduced pathogenicity once infected, through recovery from infection and through remaining immune to infection: acquired immunity. We assume that each of these mechanisms is costly to the host and find that the evolutionary dynamics of innate immunity in hosts that also have acquired immunity are quantitatively the same as in hosts that possess only innate immunity. However, compared with resistance through avoidance or recovery, there is less likely to be polymorphism in the length of acquired immunity within populations. Long-lived organisms that can recover at intermediate rates faced with fast-transmitting pathogens that cause intermediate pathogenicity (mortality of infected individuals) are most likely to evolve long-lived acquired immunity. Our work emphasizes that because whether or not acquired immunity is beneficial depends on the characteristics of the disease, organisms may be selected to only develop acquired immunity to some of the diseases that they encounter

The Need for Evolutionarily Rational Disease Interventions: Vaccination Can Select for Higher Virulence

This is the final version of the article. Available from Public Library of Science via the DOI in this recordThere is little doubt evolution has played a major role in preventing the control of infectious disease through antibiotic and insecticide resistance, but recent theory suggests disease interventions such as vaccination may lead to evolution of more harmful parasites. A new study published in PLOS Biology by Andrew Read and colleagues shows empirically that vaccination against Marek's disease has favored higher virulence; without intervention, the birds die too quickly for any transmission to occur, but vaccinated hosts can both stay alive longer and shed the virus. This is an elegant empirical demonstration of how evolutionary theory can predict potentially dangerous responses of infectious disease to human interventions

The evolution of oscillatory behavior in age-structured species

A major challenge in ecology is to explain why so many species show oscillatory population dynamics and why the oscillations commonly occur with particular periods. The background environment, through noise or seasonality, is one possible driver of these oscillations, as are the components of the trophic web with which the species interacts. However, the oscillation may also be intrinsic, generated by density-dependent effects on the life history. Models of structured single-species systems indicate that a much broader range of oscillatory behavior than that seen in nature is theoretically possible. We test the hypothesis that it is selection that acts to constrain the range of periods. We analyze a nonlinear single-species matrix model with density dependence affecting reproduction and with trade-offs between reproduction and survival. We show that the evolutionarily stable state is oscillatory and has a period roughly twice the time to maturation, in line with observed patterns of periodicity. The robustness of this result to variations in trade-off function and density dependence is tested

Accommodating Complex Substitution Patterns in a Random Utility Model of Recreational Fishing

We employed a cross-nested logit (CNL) model that permits a rich pattern of substitution among alternatives within a closed form choice model. The specification we employed is ideal for applications with many choice alternatives, such as the 431 fishing sites in this application. The CNL model provided a significant improvement over multinomial and nested logit model specifications at explaining observed recreational fishing site choices by residents of northern Ontario, Canada. Results from two scenarios illustrated the implications of using the CNL model on spatial substitution patterns and welfare measures associated with attribute change scenarios. The CNL model forecasts demonstrated that the relative change in fishing site use was lower at the most affected sites and higher at sites near the affected sites than was predicted by the multinomial logit model. No consistent pattern was found in mean or variance of welfare estimates associated with hypothetical attribute changes.Compensating variation, cross-nested logit, fishing site choice, random utility model, spatial substitution, Demand and Price Analysis, Institutional and Behavioral Economics, Q26,

Using evolution to generate sustainable malaria control with spatial repellents.

Published onlineJournal ArticleThis is the final version of the article. Available from eLife Sciences Publications via the DOI in this record.Evolution persistently undermines vector control programs through insecticide resistance. Here we propose a novel strategy which instead exploits evolution to generate and sustain new control tools. Effective spatial repellents are needed to keep vectors out of houses. Our approach generates such new repellents by combining a high-toxicity insecticide with a candidate repellent initially effective against only part of the vector population. By killing mosquitoes that enter treated properties the insecticide selects for vector phenotypes deflected by the repellent, increasing efficacy of the repellent against the target vector population and in turn protecting the insecticide against the spread of insecticide resistance. Using such evolved spatial repellents offers an evolutionarily sustainable, 'double-dip' system of disease control combining mortality and repellence. We formalize this idea using models which explore vector population genetics and disease transmission probabilities and show that using evolved spatial repellents is theoretically achievable, effective and sustainable.Biotechnology and Biological Sciences Research Council BB/L010879/1 NERC Environmental Bioinformatics Centre NE/J009784/

The interaction of seasonal forcing and immunity and the resonance dynamics of malaria

This is the final version of the article. Available from the Royal Society via the DOI in this recordTheory has emphasized the importance of both intrinsic factors such as host immunity and extrinsic drivers such as climate in determining disease dynamics. In particular, seasonality may lead to multi-annual cycles in prevalence, but the likelihood of this depends on the role of acquired immunity. Some diseases including malaria have immunity that falls between the classic susceptible-infectious-removed and susceptible-infectious-susceptible models. Here, we investigate the general conditions promoting the subharmonic resonance behaviour that may lead to multi-annual cycles in a general malaria dynamical model. Utilizing two complementary approaches to bifurcation analyses, we show that resonance is promoted by processes shortening the length of the infectious period and that subharmonic cycles are favoured in situations with strong seasonality in transmission but at intermediate levels of endemicity. We discuss the implications of our results for understanding prevalence patterns in long-term malaria datasets from Kenya that show multi-annual cycles and one from Thailand that does not and discuss the possible implications of treatment.This work was supported by the award of a Leverhulme Early Career Research Fellowship to D.Z.C. and a Welcome Trust VIP grant M.B

Coevolution of parasite virulence and host mating strategies

This is the author accepted manuscript. The final version is available from National Academy of Sciences via the DOI in this record.Parasites are thought to play an important role in sexual selection and the evolution of mating strategies, which in turn are likely to be critical to the transmission and therefore the evolution of parasites. Despite this clear interdependence we have little understanding of parasite-mediated sexual selection in the context of reciprocal parasite evolution. Here we develop a general coevolutionary model between host mate preference and the virulence of a sexually transmitted parasite. We show when the characteristics of both the host and parasite lead to coevolutionarily stable strategies or runaway selection, and when coevolutionary cycling between high and low levels of host mate choosiness and virulence is possible. A prominent argument against parasites being involved in sexual selection is that they should evolve to become less virulent when transmission depends on host mating success. The present study, however, demonstrates that coevolution can maintain stable host mate choosiness and parasite virulence or indeed coevolutionary cycling of both traits. We predict that choosiness should vary inversely with parasite virulence and that both relatively long and short life spans select against choosy behavior in the host. The model also reveals that hosts can evolve different behavioral responses from the same initial conditions, which highlights difficulties in using comparative analysis to detect parasite-mediated sexual selection. Taken as a whole, our results emphasize the importance of viewing parasite-mediated sexual selection in the context of coevolution.Funding for this work was provided by the Natural Environment Research Council (Grant NE/K014617/1) and a Biotechnology and Biological Sciences Research Council studentship

The Role of Trade-off Shapes in the Evolution of Parasites in Spatial Host Populations: An Approximate Analytical Approach

Given the substantial changes in mixing in many populations, there is considerable interest in the role that spatial structure can play in the evolution of disease. Here we examine the role of different trade-off shapes in the evolution of parasites in a spatially structured host population where infection can occur locally or globally. We develop an approximate adaptive dynamic analytical approach, to examine how the evolutionarily stable (ES) virulence depends not only on the fraction of global infection/transmission but also on the shape of the trade-off between transmission and virulence. Our analysis can successfully predict the ES virulence found previously by simulation of the full system. The analysis confirms that when there is a linear trade-off between transmission and virulence spatial structure may lead to an ES virulence that increases as the proportion of global transmission increases. However, we also show that the ESS disappears above a threshold level of global infection, leading to maximization. In addition just below this threshold, there is the possibility of evolutionary bi-stabilities. When we assume the realistic trade-off between transmission and virulence that results in an ESS in the classical mixed model, we find that spatial structure can increase or decrease the ES virulence. A relatively high proportion of local infection reduces virulence but intermediate levels can select for higher virulence. Our work not only emphasizes the importance of spatial structure to the evolution of parasites, but also makes it clear that situations between the local and the global need to be considered. We also emphasize the key role that the shape of trade-offs plays in evolutionary outcomes

The Role of Trade-off Shapes in the Evolution and Coexistence of Virulence in Spatial Host-Parasite Interactions: An Approximate Adaptive Dynamical Approach

We propose a new analysis for the evolution of virulence of pathogen in a spatially structured host population where each site of a regular lattice is either occupied by a susceptible or by an infected, or is empty. We assume that reproduction by susceptible individuals occurs locally but infection by a contact of susceptible and infected hosts occurs either locally or globally with a certain proportion. We examine by combining Monte-Carlo simulation and adaptive dynamics approach, how the evolutionarily stable (ESS) virulence depends on the fraction of global infection/transmission and the trade-off between transmission and virulence in the model investigated by Boots and Sasaki (1999). Our analysis developed in this paper can successfully predicted the ESS virulence found in the previous papers, and reveals followings: [1] With a linear trade-off, as is reported by previous studies, there is an ESS virulence when the proportion of global infection is small. We newly find that, if we increase the proportion, the ESS disappears when the proportion exceeds a certain threshold value, and proportions just below the threshold, there are evolutionary bi-stabilities. [2] With a non-linear trade-off, there can be no monomorphic ESS; instead, the evolutionary competition between many parasite genotypes differing in their virulence gives rise to an evolutionarily stable coalition of pathogen strains with markedly different virulence (dimorphic ESS virulence) with a middle proportion of global transmission. These analytical results well illustrate the results by Monte-Carlo simulations. Since coexistence and evolutionary bistability are not impossible in the model we investigate in this paper, these are apparently derived by the effect of spatial structure