Social interactions modulate the virulence of avian malaria infection

There is an increasing understanding of the context-dependent nature of parasite virulence. Variation in parasite virulence can occur when infected individuals compete with conspecifics that vary in infection status; virulence may be higher when competing with uninfected competitors. In vertebrates with social hierarchies, we propose that these competition-mediated costs of infection may also vary with social status. Dominant individuals have greater competitive ability than competing subordinates, and consequently may pay a lower prevalence-mediated cost of infection. In this study we investigated whether costs of malarial infection were affected by the occurrence of the parasite in competitors and social status in domestic canaries (Serinus canaria). We predicted that infected subordinates competing with non-infected dominants would pay higher costs than infected subordinates competing with infected dominants. We also predicted that these occurrence-mediated costs of infection would be ameliorated in infected dominant birds. We found that social status and the occurrence of parasites in competitors significantly interacted to change haematocrit in infected birds. Namely, subordinate and dominant infected birds differed in haematocrit depending on the infection status of their competitors. However, in contrast to our prediction, dominants fared better with infected subordinates, whereas subordinates fared better with uninfected dominants. Moreover, we found additional effects of parasite occurrence on mortality in canaries. Ultimately, we provide evidence for costs of parasitism mediated by social rank and the occurrence of parasites in competitors in a vertebrate species. This has important implications for our understanding of the evolutionary processes that shape parasite virulence and group living.     

Host age modulates within-host parasite competition

In many host populations, one of the most striking differences among hosts is their age. While parasite prevalence differences in relation to host age are well known, little is known on how host age impacts ecological and evolutionary dynamics of diseases. Using two clones of the water flea Daphnia magna and two clones of its bacterial parasite Pasteuria ramosa, we examined how host age at exposure influences within-host parasite competition and virulence. We found that multiply-exposed hosts were more susceptible to infection and suffered higher mortality than singly-exposed hosts. Hosts oldest at exposure were least often infected and vice versa. Furthermore, we found that in young multiply-exposed hosts competition was weak, allowing coexistence and transmission of both parasite clones, whereas in older multiply-exposed hosts competitive exclusion was observed. Thus, age-dependent parasite exposure and host demography (age structure) could together play an important role in mediating parasite evolution. At the individual level, our results demonstrate a previously unnoticed interaction of the host''s immune system with host age, suggesting that the specificity of immune function changes as hosts mature. Therefore, evolutionary models of parasite virulence might benefit from incorporating age-dependent epidemiological parameters.     

Within-host Competition Does Not Select for Virulence in Malaria Parasites; Studies with Plasmodium yoelii

In endemic areas with high transmission intensities, malaria infections are very often composed of multiple genetically distinct strains of malaria parasites. It has been hypothesised that this leads to intra-host competition, in which parasite strains compete for resources such as space and nutrients. This competition may have repercussions for the host, the parasite, and the vector in terms of disease severity, vector fitness, and parasite transmission potential and fitness. It has also been argued that within-host competition could lead to selection for more virulent parasites. Here we use the rodent malaria parasite Plasmodium yoelii to assess the consequences of mixed strain infections on disease severity and parasite fitness. Three isogenic strains with dramatically different growth rates (and hence virulence) were maintained in mice in single infections or in mixed strain infections with a genetically distinct strain. We compared the virulence (defined as harm to the mammalian host) of mixed strain infections with that of single infections, and assessed whether competition impacted on parasite fitness, assessed by transmission potential. We found that mixed infections were associated with a higher degree of disease severity and a prolonged infection time. In the mixed infections, the strain with the slower growth rate was often responsible for the competitive exclusion of the faster growing strain, presumably through host immune-mediated mechanisms. Importantly, and in contrast to previous work conducted with Plasmodium chabaudi, we found no correlation between parasite virulence and transmission potential to mosquitoes, suggesting that within-host competition would not drive the evolution of parasite virulence in P. yoelii.     

Of mice and worms: are co-infections with unrelated parasite strains more damaging to definitive hosts?

Intraspecific competition between co-infecting parasites can influence the amount of virulence, or damage, they do to their host. Kin selection theory dictates that infections with related parasite individuals should have lower virulence than infections with unrelated individuals, because they benefit from inclusive fitness and increased host longevity. These predictions have been tested in a variety of microparasite systems, and in larval stage macroparasites within intermediate hosts, but the influence of adult macroparasite relatedness on virulence has not been investigated in definitive hosts. This study used the human parasite Schistosoma mansoni to determine whether definitive hosts infected with related parasites experience lower virulence than hosts infected with unrelated parasites, and to compare the results from intermediate host studies in this system. The presence of unrelated parasites in an infection decreased parasite infectivity, the ability of a parasite to infect a definitive host, and total worm establishment in hosts, impacting the less virulent parasite strain more severely. Unrelated parasite co-infections had similar virulence to the more virulent of the two parasite strains. We combine these findings with complementary studies of the intermediate snail host and describe trade-offs in virulence and selection within the life cycle. Damage to the host by the dominant strain was muted by the presence of a competitor in the intermediate host, but was largely unaffected in the definitive host. Our results in this host–parasite system suggest that unrelated infections may select for higher virulence in definitive hosts while selecting for lower virulence in intermediate hosts.     

Are Sick Individuals Weak Competitors? Competitive Ability of Snails Parasitized by a Gigantism-Inducing Trematode

Parasitized individuals are often expected to be poor competitors because they are weakened by infections. Many trematode species, however, although extensively exploiting their mollusc hosts, also induce gigantism (increased host size) by diverting host resources towards growth instead of reproduction. In such systems, alternatively to reduced competitive ability due to negative effects of parasitism on host performance, larger size could allow more efficient resource acquisition and thus increase the relative competitive ability of host individuals. We addressed this hypothesis by testing the effect of a trematode parasite Diplostomum pseudospathaceum on the competitive ability of its snail host Lymnaea stagnalis. We experimentally examined the growth of snails kept in pairs in relation to their infection status and intensity of resource competition (i.e. food availability). We found that parasitized snails grew faster and their reproduction was reduced compared to unparasitized individuals indicating parasite-induced gigantism. However, growth of the snails was faster when competing with parasitized individuals compared to unparasitized snails indicating reduced competitive ability due to parasitism. The latter effect, however, was relatively weak suggesting that the effects of the parasite on snail physiology may partly override each other in determining competitive ability.     

Mallards Feed Longer to Maintain Intake Rate under Competition on a Natural Food Distribution

Animals foraging in groups may benefit from a faster detection of food and predators, but competition by conspecifics may reduce intake rate. Competition may also alter the foraging behaviour of individuals, which can be influenced by dominance status and the way food is distributed over the environment. Many studies measuring the effects of competition and dominance status have been conducted on a uniform or highly clumped food distribution, while in reality prey distributions are often in‐between these two extremes. The few studies that used a more natural food distribution only detected subtle effects of interference and dominance. We therefore conducted an experiment on a natural food distribution with focal mallards Anas platyrhynchos foraging alone and in a group of three, having a dominant, intermediate or subordinate dominance status. In this way, the foraging behaviour of the same individual in different treatments could be compared, and the effect of dominance was tested independently of individual identity. The experiment was balanced using a 4 × 4 Latin square design, with four focal and six non‐focal birds. Individuals in a group achieved a similar intake rate (i.e. number of consumed seeds divided by trial length) as when foraging alone, because of an increase in the proportion of time feeding (albeit not significant for subordinate birds). Patch residence time and the number of different patches visited did not differ when birds were foraging alone or in a group. Besides some agonistic interactions, no differences in foraging behaviour between dominant, intermediate and subordinate birds were measured in group trials. Possibly group‐foraging birds increased their feeding time because there was less need for vigilance or because they increased foraging intensity to compensate for competition. This study underlines that a higher competitor density does not necessarily lead to a lower intake rate, irrespective of dominance status.     

Interactions among bacterial strains and fluke genotypes shape virulence of co-infection

Most studies of virulence of infection focus on pairwise host–parasite interactions. However, hosts are almost universally co-infected by several parasite strains and/or genotypes of the same or different species. While theory predicts that co-infection favours more virulent parasite genotypes through intensified competition for host resources, knowledge of the effects of genotype by genotype (G × G) interactions between unrelated parasite species on virulence of co-infection is limited. Here, we tested such a relationship by challenging rainbow trout with replicated bacterial strains and fluke genotypes both singly and in all possible pairwise combinations. We found that virulence (host mortality) was higher in co-infections compared with single infections. Importantly, we also found that the overall virulence was dependent on the genetic identity of the co-infecting partners so that the outcome of co-infection could not be predicted from the respective virulence of single infections. Our results imply that G × G interactions among co-infecting parasites may significantly affect host health, add to variance in parasite fitness and thus influence evolutionary dynamics and ecology of disease in unexpected ways.     

Heterogeneous interspecific interactions in a host-parasite system

Macroparasites of vertebrates usually occur in multi-species communities, producing infections whose outcome in individual hosts or host populations may depend on the dynamics of interactions amongst the different component species. Within a single co-infection, competition can occur between conspecific and heterospecific parasite individuals, either directly or via the host's physiological and immune responses. We studied a natural single-host, multi-parasite model infection system (polystomes in the anuran Xenopus laevis victorianus) in which the parasite species show total interspecific competitive exclusion as adults in host individuals. Multi-species infection experiments indicated that competitive outcomes were dependent on infection species composition and strongly influenced by the intraspecific genetic identity of the interacting organisms. Our results also demonstrate the special importance of temporal heterogeneity (the sequence of infection by different species) in competition and co-existence between parasite species and predict that developmental plasticity in inferior competitors, and the induction of species-specific host resistance, will partition the within-host-individual habitat over time. We emphasise that such local (within-host) context-dependent processes are likely to be a fundamental determinant of population dynamics in multi-species parasite assemblages.     

House sparrows (Passer domesticus) adjust their social status position to their physiological costs

For group-living animals, the maintenance of a position in the social hierarchy may be associated with physiological costs such as increased stress and energy expenditure or suppressed immune functions. In this study, we experimentally manipulated the social status of house sparrows so that each bird experienced two social environments in random sequence: being dominant and subordinate. For 14 males, we investigated how corticosterone concentrations, energy expenditure and immune functions were affected by these changes in social status position. We found that the cost of maintaining a social status position differed between individuals and were related to individual body size. Birds with small body size had increased costs in terms of increased stress responses and reduced cell-mediated immune responses while being experimentally kept as dominants, while birds with large body size had increased costs while they were subordinates. We also found that birds with increased energetic and immunological costs as dominants obtained a low status position in the large group, while birds with increased costs as subordinates obtained a high status position in the large group. In summary, we found that the costs associated with the maintenance of social status position differed between individuals and was related to the individuals' body size. Furthermore, in a large group, individuals maintained a social status position that minimized energetic and immunological costs.     

Host exposure history and priority effects impact the development and reproduction of a dominant parasite

Within a single organism, numerous parasites often compete for space and resources. This competition, together with a parasite’s ability to locate and successfully establish in a host, can contribute to the distribution and prevalence of parasites. Coinfection with trematodes in snail intermediate hosts is rarely observed in nature, partly due to varying competitive abilities among parasite taxa. Using a freshwater snail host (Biomphalaria glabrata), we studied the ability of a competitively dominant trematode, Echinostoma caproni, to establish and reproduce in a host previously infected with a less competitive trematode species, Schistosoma mansoni. Snails were exposed to S. mansoni and co-exposed to E. caproni either simultaneously or 1 week, 4 weeks, or 6 weeks post S. mansoni exposure. Over the course of infection, we monitored the competitive success of the dominant trematode through infection prevalence, parasite development time, and parasite reproductive output. Infection prevalence of E. caproni did not differ among co-exposed groups or between co-exposed and single exposed groups. However, E. caproni infections in co-exposed hosts took longer to reach maturity when the timing between co-exposures increased. All co-exposed groups had higher E. caproni reproductive output than single exposures. We show that although timing of co-exposure affects the development time of parasite transmission stages, it is not important for successful establishment. Additionally, co-exposure, but not priority effects, increases the reproductive output of the dominant parasite.     

Virulence and competitive ability in an obligately killing parasite

Mixed infections are thought to have a major influence on the evolution of parasite virulence. During a mixed infection, higher within‐host parasite growth is favored under the assumption that it is critical to the competitive success of the parasite. As within‐host parasite growth may also increase damage to the host, a positive correlation is predicted between virulence and competitive success. However, when parasites must kill their hosts in order be transmitted, parasites may spend energy on directly attacking their host, even at the cost of their within‐host growth. In such systems, a negative correlation between virulence and competitive success may arise. We examined virulence and competitive ability in three sympatric species of obligately killing nematode parasites in the genus Steinernema. These nematodes exist in a mutualistic symbiosis with bacteria in the genus Xenorhabdus. Together the nematodes and their bacteria kill the insect host soon after infection, with reproduction of both species occurring mainly after host death. We found significant differences among the three nematode species in the speed of host killing. The nematode species with the lowest and highest levels of virulence were associated with the same species of Xenorhabdus, indicating that nematode traits, rather than the bacterial symbionts, may be responsible for the differences in virulence. In mixed infections, host mortality rate closely matched that associated with the more virulent species, and the more virulent species was found to be exclusively transmitted from the majority of coinfected hosts. Thus, despite the requirement of rapid host death, virulence appears to be positively correlated with competitive success in this system. These findings support a mechanistic link between parasite growth and both anti‐competitor and anti‐host factors.     

Social network structure and parasite infection patterns in a territorial reptile, the tuatara (Sphenodon punctatus)

We investigated whether the parasite load of an individual could be predicted by its position in a social network. Specifically, we derived social networks in a solitary, territorial reptile (the tuatara, Sphenodon punctatus), with links based on the sharing of space, not necessarily synchronously, in overlapping territories. Tuatara are infected by ectoparasitic ticks (Amblyomma sphenodonti), mites (Neotrombicula spp.) and a blood parasite (Hepatozoon tuatarae) which is transmitted by the tick. We recorded the location of individual tuatara in two study plots twice daily during the mating season (March) in 2 years (2006 and 2007) on Stephens Island, New Zealand. We constructed weighted, directed networks to represent pathways for parasite transmission, where nodes represented individual tuatara and edges connecting the nodes represented the extent of territory overlap among each pair of individuals. We considered a network-based hypothesis which predicted that the in-strength of individuals (the sum of edge weights directed towards a node) in the derived network would be positively related to their parasite load. Alternatively, if the derived social network did not reflect actual parasite transmission, we predicted other factors such as host sex, size or territory size may better explain variation in parasite infection patterns. We found clear positive relationships between the in-strength of tuatara and their tick loads, and infection patterns with tick-borne blood parasites. In particular, the extent that individuals were connected to males in the network consistently predicted tick loads of tuatara. However, mite loads of tuatara were significantly related to host sex, body size and territory size, and showed little association with network measures. The results suggest that the pathway of transmission of parasites through a population will depend on the transmission mechanism of the parasite, but that social networks provide a powerful predictive tool for some parasites.     

Ontogeny of food-caching site preferences in young Florida Scrub-Jays: evidence of learning or changing social status?

Florida Scrub-Jays (Aphelocoma coerulescens) are cooperative breeders endemic to Florida’s oak scrub. In autumn, Florida Scrub-Jays cache thousands of acorns and exhibit behaviors that appear to balance cache site selection against food degradation or cache robbery. However, both experience and position within a social dominance hierarchy could affect individual cache preferences. We examined the cache site preferences of birds with differing levels of caching experience and at different strata within a complex social dominance hierarchy. Our objective was to determine how experience, social position, and social context when caching influenced microhabitat preferences, and if these change as jays age, gain experience, and their social position changes. Naïve first-year birds preferred to cache in well-hidden, densely vegetated sites with relatively high soil moisture content. Naïve birds also cached farther from provisioning points if observed by a socially dominant bird than when they were alone or in the presence of birds of equal social status. Experienced adults preferred to cache in open, dry sandy sites and social context at the time of caching did not influence their preferences. As naïve birds aged, they gained experience and their social position changed. Experienced second-year birds shifted their preference to more open, drier sites, and did so more often when they remained subordinate within their group rather than becoming dominant breeders. Second-year birds that remained subordinate did not alter their caching behavior if observed by dominant birds. These patterns suggest that after gaining experience, jays learned which sites were more appropriate for caching and shifted their preference, regardless of their changing social status. We suggest that the risk of cache loss to food degradation might be greater than the risk of pilfering for Florida Scrub-Jays, especially for birds in any social strata except the most subordinate, but this requires additional study.     

Intensive aquaculture selects for increased virulence and interference competition in bacteria

Although increased disease severity driven by intensive farming practices is problematic in food production, the role of evolutionary change in disease is not well understood in these environments. Experiments on parasite evolution are traditionally conducted using laboratory models, often unrelated to economically important systems. We compared how the virulence, growth and competitive ability of a globally important fish pathogen, Flavobacterium columnare, change under intensive aquaculture. We characterized bacterial isolates from disease outbreaks at fish farms during 2003–2010, and compared F. columnare populations in inlet water and outlet water of a fish farm during the 2010 outbreak. Our data suggest that the farming environment may select for bacterial strains that have high virulence at both long and short time scales, and it seems that these strains have also evolved increased ability for interference competition. Our results are consistent with the suggestion that selection pressures at fish farms can cause rapid changes in pathogen populations, which are likely to have long-lasting evolutionary effects on pathogen virulence. A better understanding of these evolutionary effects will be vital in prevention and control of disease outbreaks to secure food production.     

Expression of parasite genetic variation changes over the course of infection: implications of within-host dynamics for the evolution of virulence

How infectious disease agents interact with their host changes during the course of infection and can alter the expression of disease-related traits. Yet by measuring parasite life-history traits at one or few moments during infection, studies have overlooked the impact of variable parasite growth trajectories on disease evolution. Here we show that infection-age-specific estimates of host and parasite fitness components can reveal new insight into the evolution of parasites. We do so by characterizing the within-host dynamics over an entire infection period for five genotypes of the castrating bacterial parasite Pasteuria ramosa infecting the crustacean Daphnia magna. Our results reveal that genetic variation for parasite-induced gigantism, host castration and parasite spore loads increases with the age of infection. Driving these patterns appears to be variation in how well the parasite maintains control of host reproduction late in the infection process. We discuss the evolutionary consequences of this finding with regard to natural selection acting on different ages of infection and the mechanism underlying the maintenance of castration efficiency. Our results highlight how elucidating within-host dynamics can shed light on the selective forces that shape infection strategies and the evolution of virulence.     

Familiarity Breeds Tolerance: the Development of Social Stability in Flocking Siskins (Carduelis spinus)

Behavioural integration associated with the fusion of two flocks is analyzed in captive siskins (Carduelis spinus) by quantifying changes in social behaviour with time since joining. In general there was an increase in the incidence of tolerant behaviour, supplanting attacks and hopping withdrawals with time since fusion of the flocks. However, the number of displays and flights showed the opposite, negative, trend. Taking dominance status into account, the greatest change in behaviour with time since joining is an increase in tolerance by dominants of new flock companions. Factorial analysis of correspondences was used to study how different birds changed their behaviour with time since joining a flock. This analysis showed that the introduction of new birds did not disrupt relationships with familiar birds, and that residents are dominant in interactions with the incoming new flock companions. The analysis also demonstrated that relationships within the new flock had stabilized 20 days after the flocks had joined. The characteristics of the socially integrated group of siskins are quite similar to those described by Rohwer & Ewald (1981) in their shepherds hypothesis: dominants tolerate their subordinates feeding in close proximity, offering them a profitable feeding area, but also supplant them to obtain food; both dominants and subordinates benefit from being in a flock. As a consequence, constant changes of membership in flocks is costly not only because birds lose dominance status, but also the advantages of clear dominant and subordinate roles.     

Host heterogeneity is a determinant of competitive exclusion or coexistence in genetically diverse malaria infections

During an infection, malaria parasites compete for limited amounts of food and enemy-free space. Competition affects parasite growth rate, transmission and virulence, and is thus important for parasite evolution. Much evolutionary theory assumes that virulent clones outgrow avirulent ones, favouring the evolution of higher virulence. We infected laboratory mice with a mixture of two Plasmodium chabaudi clones: one virulent, the other avirulent. Using real-time quantitative PCR to track the two parasite clones over the course of the infection, we found that the virulent clone overgrew the avirulent clone. However, host genotype had a major effect on the outcome of competition. In a relatively resistant mouse genotype (C57B1/6J), the avirulent clone was suppressed below detectable levels after 10 days, and apparently lost from the infection. By contrast, in more susceptible mice (CBA/Ca), the avirulent clone was initially suppressed, but it persisted, and during the chronic phase of infection it did better than it did in single infections. Thus, the qualitative outcome of competition depended on host genotype. We suggest that these differences may be explained by different immune responses in the two mouse strains. Host genotype and resistance could therefore play a key role in the outcome of within-host competition between parasite clones and in the evolution of parasite virulence.     

Differential Tolerance to Direct and Indirect Density-Dependent Costs of Viral Infection in Arabidopsis thaliana

Population density and costs of parasite infection may condition the capacity of organisms to grow, survive and reproduce, i.e. their competitive ability. In host–parasite systems there are different competitive interactions: among uninfected hosts, among infected hosts, and between uninfected and infected hosts. Consequently, parasite infection results in a direct cost, due to parasitism itself, and in an indirect cost, due to modification of the competitive ability of the infected host. Theory predicts that host fitness reduction will be higher under the combined effects of costs of parasitism and competition than under each factor separately. However, experimental support for this prediction is scarce, and derives mostly from animal–parasite systems. We have analysed the interaction between parasite infection and plant density using the plant-parasite system of Arabidopsis thaliana and the generalist virus Cucumber mosaic virus (CMV). Plants of three wild genotypes grown at different densities were infected by CMV at various prevalences, and the effects of infection on plant growth and reproduction were quantified. Results demonstrate that the combined effects of host density and parasite infection may result either in a reduction or in an increase of the competitive ability of the host. The two genotypes investing a higher proportion of resources to reproduction showed tolerance to the direct cost of infection, while the genotype investing a higher proportion of resources to growth showed tolerance to the indirect cost of infection. Our findings show that the outcome of the interaction between host density and parasitism depends on the host genotype, which determines the plasticity of life-history traits and consequently, the host capacity to develop different tolerance mechanisms to the direct or indirect costs of parasitism. These results indicate the high relevance of host density and parasitism in determining the competitive ability of a plant, and stress the need to simultaneously consider both factors to understand the selective pressures that drive host–parasite co-evolution.     

Experimentally increased social competition compromises humoral immune responses in house finches

Although social behavior can substantially influence an individual's physiology, few studies have examined whether intraspecific competition compromises individual immunocompetence. We experimentally manipulated the intensity of social competition in captive non-breeding house finches (Carpodacus mexicanus) by supplying few (high competition) or many (low competition) feeding sites. We tested whether elevated levels of social competition caused individual changes in aggression rates, humoral immunity, body mass, and baseline and stress-induced corticosterone concentrations. We also examined whether physiological responses to social competition were related to an individual's social status. We found that house finches under high social competition had significantly higher aggression rates, lower antibody responses, and lost more body mass. Within flocks, dominant individuals mounted stronger immune responses in both competition treatments. Our statistical power to detect differences in circulating corticosterone concentrations was low, but we did not find any support for the hypothesis that corticosterone concentrations mediate immunosuppression among or within flocks: baseline and stress-induced corticosterone concentrations did not differ under high and low social competition, were unrelated to individual social status, and did not predict the extent of immunosuppression among individuals. Overall, we documented that two universal components of social behavior, intraspecific competition and social status, modulated the strength of a humoral immune response in house finches.     

Superinfection and the coevolution of parasite virulence and host recovery

Parasite strategies of host exploitation may be affected by host defence strategies and multiple infections. In particular, within‐host competition between multiple parasite strains has been shown to select for higher virulence. However, little is known on how multiple infections could affect the coevolution between host recovery and parasite virulence. Here, we extend a coevolutionary model introduced by van Baalen (Proc. R. Soc. B, 265, 1998, 317) to account for superinfection. When the susceptibility to superinfection is low, we recover van Baalen's results and show that there are two potential evolutionary endpoints: one with avirulent parasites and poorly defended hosts, and another one with high virulence and high recovery. However, when the susceptibility to superinfection is above a threshold, the only possible evolutionary outcome is one with high virulence and high investment into defence. We also show that within‐host competition may select for lower host recovery, as a consequence of selection for more virulent strains. We discuss how different parasite and host strategies (superinfection facilitation, competitive exclusion) as well as demographic and environmental parameters, such as host fecundity or various costs of defence, may affect the interplay between multiple infections and host–parasite coevolution. Our model shows the interplay between coevolutionary dynamics and multiple infections may be affected by crucial mechanistic or ecological details.