Plant biologists have long recognized that host defence against parasites and pathogens can be divided into two conceptually different components: the ability to limit parasite burden (resistance) and the ability to limit the harm caused by a given burden (tolerance). Together these two components determine how well a host is protected against the effects of parasitism. This distinction is useful because it recognizes that hosts that are best at controlling parasite burdens are not necessarily the healthiest. Moreover, resistance and tolerance can be expected to have different effects on the epidemiology of infectious diseases and host-parasite coevolution. However, studies of defence in animals have to date focused on resistance, whereas the possibility of tolerance and its implications have been largely overlooked. The aim of our review is to (i) describe the statistical framework for analysis of tolerance developed in plant science and how this can be applied to animals, (ii) review evidence of genetic and environmental variation for tolerance in animals, and studies indicating which mechanisms could contribute to this variation, and (iii) outline avenues for future research on this topic.
Hosts can in principle employ two different strategies to defend themselves against parasites: resistance and tolerance. Animals typically exhibit considerable genetic variation for resistance (the ability to limit parasite burden). However, little is known about whether animals can evolve tolerance (the ability to limit the damage caused by a given parasite burden). Using rodent malaria in laboratory mice as a model system and the statistical framework developed by plant-pathogen biologists, we demonstrated genetic variation for tolerance, as measured by the extent to which anemia and weight loss increased with increasing parasite burden. Moreover, resistance and tolerance were negatively genetically correlated. These results mean that animals, like plants, can evolve two conceptually different types of defense, a finding that has important implications for the understanding of the epidemiology and evolution of infectious diseases.
Vaccines rarely provide full protection from disease. Nevertheless, partially effective (imperfect) vaccines may be used to protect both individuals and whole populations. We studied the potential impact of different types of imperfect vaccines on the evolution of pathogen virulence (induced host mortality) and the consequences for public health. Here we show that vaccines designed to reduce pathogen growth rate and/or toxicity diminish selection against virulent pathogens. The subsequent evolution leads to higher levels of intrinsic virulence and hence to more severe disease in unvaccinated individuals. This evolution can erode any population-wide benefits such that overall mortality rates are unaffected, or even increase, with the level of vaccination coverage. In contrast, infection-blocking vaccines induce no such effects, and can even select for lower virulence. These findings have policy implications for the development and use of vaccines that are not expected to provide full immunity, such as candidate vaccines for malaria.
Microparasite infections often consist of genetically distinct clonal lineages. Ecological interactions between these lineages within hosts can influence disease severity, epidemiology, and evolution. Many medical and veterinary interventions have an impact on genetic diversity within infections, but there is little understanding of the long-term consequences of such interventions for public and animal health. Indeed, much of the theory in this area is based on assumptions contradicted by the available data.
Malaria transmission is strongly influenced by environmental temperature, but the biological drivers remain poorly quantified. Most studies analyzing malaria-temperature relations, including those investigating malaria risk and the possible impacts of climate change, are based solely on mean temperatures and extrapolate from functions determined under unrealistic laboratory conditions. Here, we present empirical evidence to show that, in addition to mean temperatures, daily fluctuations in temperature affect parasite infection, the rate of parasite development, and the essential elements of mosquito biology that combine to determine malaria transmission intensity. In general, we find that, compared with rates at equivalent constant mean temperatures, temperature fluctuation around low mean temperatures acts to speed up rate processes, whereas fluctuation around high mean temperatures acts to slow processes down. At the extremes (conditions representative of the fringes of malaria transmission, where range expansions or contractions will occur), fluctuation makes transmission possible at lower mean temperatures than currently predicted and can potentially block transmission at higher mean temperatures. If we are to optimize control efforts and develop appropriate adaptation or mitigation strategies for future climates, we need to incorporate into predictive models the effects of daily temperature variation and how that variation is altered by climate change.Anopheles mosquitoes | climate change | diurnal temperature variability | ectotherms | Plasmodium malaria T he basic reproductive number (R 0 ), which defines the number of cases of a disease that arise from one case of the disease introduced into a population of susceptible hosts, is a key epidemiological metric providing essential information for understanding disease risk and for targeting resources for control. For malaria, R 0 is commonly described by the formula R 0 = ma 2 bce −pS /pr [note that this expression is also defined as (R 0 ) 2 ; ref. 1], where m is the vector:human ratio, a vector biting frequency, bc transmission coefficients defining vector competence, p daily vector survival rate, S the extrinsic incubation or development period of the parasite within the vector, and r the recovery rate of the vertebrate hosts from infection. Given that six of seven of these parameters relate in some way to mosquito abundance, biology, or physiology and that mosquitoes are small cold-blooded insects, it is clear that the transmission intensity of malaria will be strongly influenced by environmental temperature (2-6). Accordingly, the dynamics and distribution of malaria are expected to be extremely sensitive to climate change, although the nature and extent of the response remains highly controversial (7-15).The standard relationships describing the effects of temperature on malaria parasite and mosquito life history derive largely from laboratory studies conducted under constant temperature conditions (e.g., ref. 2 and references therein) and tend to use ...
Several epidemiological models predict a positive relationship between host population density and abundance of directly transmitted macroparasites. Here, we generalize these, and test the prediction by a comparative study. We used data on communities of gastrointestinal strongylid nematodes from 19 mammalian species, representing examination of 6670 individual hosts. We studied both the average abundance of all strongylid nematodes within a host species, and the two components of abundance, prevalence and intensity. The e¡ects of host body weight, diet, fecundity and age at maturity and parasite body size were controlled for directly, and the phylogenetically independent contrast method was used to control for confounding factors more generally. Host population density and average parasite abundance were strongly positively correlated within mammalian taxa, and across all species when the e¡ects of host body weight were controlled for. Controlling for other variables did not change this. Even when looking at single parasite species occurring in several host species, abundance was highest in the host species with the highest population density. Prevalence and intensity showed similar patterns. These patterns provide the ¢rst macroecological evidence consistent with the prediction that transmission rates depend on host population density in natural parasite communities.
Explaining parasite virulence is a great challenge for evolutionary biology. Intuitively, parasites that depend on their hosts for their survival should be benign to their hosts, yet many parasites cause harm. One explanation for this is that within-host competition favors virulence, with more virulent strains having a competitive advantage in genetically diverse infections. This idea, which is well supported in theory, remains untested empirically. Here we provide evidence that within-host competition does indeed select for high parasite virulence. We examine the rodent malaria Plasmodium chabaudi in laboratory mice, a parasite-host system in which virulence can be easily monitored and competing strains quantified by using strain-specific real-time PCR. As predicted, we found a strong relationship between parasite virulence and competitive ability, so that more virulent strains have a competitive advantage in mixed-strain infections. In transmission experiments, we found that the strain composition of the parasite populations in mosquitoes was directly correlated with the composition of the bloodstage parasite population. Thus, the outcome of within-host competition determined relative transmission success. Our results imply that within-host competition is a major factor driving the evolution of virulence and can explain why many parasites harm their hosts.competition ͉ evolution ͉ parasite ͉ Plasmodium ͉ mixed infection E xplaining virulence is fundamental to understanding the life history of parasites, arguably the most abundant group of creatures on the planet (1). The problem is to explain why parasites, which rely on their hosts for survival and fitness, should cause disease or indeed kill their hosts (2-6). Many explanations of parasite virulence have been put forward (3, 4), but the idea that has received the most attention is that virulence is a consequence of a parasite's efforts to maximize its fitness: parasites require extensive within-host replication to achieve transmission to the next host, but at the same time such replication damages host tissues, increasing the chances of killing the host (2, 3, 7-9). Higher levels of virulence than predicted by this model, however, could arise due to within-host competition between parasite strains (9-14). Many, if not most, parasite infections consist of genetically distinct strains of the same parasite species or contain virulent mutants that have arisen de novo (15). It is generally assumed that parasites that exploit their hosts prudently suffer great fitness losses in hosts simultaneously infected with more aggressive parasites. This is because virulent parasites could kill the host or competitively exclude prudent parasites before the latter have realized transmission. Even though host death also reduces the fitness of virulent parasites, prudent parasites suffer disproportionately and are eliminated by natural selection, a process commonly known as ''the tragedy of the commons'' (16).Several authors (17, 18) have gone so far as to claim that reducing t...
The incubation period for malaria parasites within the mosquito is exquisitely temperature-sensitive, so that temperature is a major determinant of malaria risk. Epidemiological models are increasingly used to guide allocation of disease control resources and to assess the likely impact of climate change on global malaria burdens. Temperature-based malaria transmission is generally incorporated into these models using mean monthly temperatures,
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