Host behaviour–parasite feedback: an essential link between animal behaviour and disease ecology

Animal behaviour and the ecology and evolution of parasites are inextricably linked. For this reason, animal behaviourists and disease ecologists have been interested in the intersection of their respective fields for decades. Despite this interest, most research at the behaviour–disease interface focuses either on how host behaviour affects parasites or how parasites affect behaviour, with little overlap between the two. Yet, the majority of interactions between hosts and parasites are probably reciprocal, such that host behaviour feeds back on parasites and vice versa. Explicitly considering these feedbacks is essential for understanding the complex connections between animal behaviour and parasite ecology and evolution. To illustrate this point, we discuss how host behaviour–parasite feedbacks might operate and explore the consequences of feedback for studies of animal behaviour and parasites. For example, ignoring the feedback of host social structure on parasite dynamics can limit the accuracy of predictions about parasite spread. Likewise, considering feedback in studies of parasites and animal personalities may provide unique insight about the maintenance of variation in personality types. Finally, applying the feedback concept to links between host behaviour and beneficial, rather than pathogenic, microbes may shed new light on transitions between mutualism and parasitism. More generally, accounting for host behaviour–parasite feedbacks can help identify critical gaps in our understanding of how key host behaviours and parasite traits evolve and are maintained.     

Parasitism and the evolutionary ecology of animal personality

The ecological factors responsible for the evolution of individual differences in animal personality (consistent individual differences in the same behaviour across time and contexts) are currently the subject of intense debate. A limited number of ecological factors have been investigated to date, with most attention focusing on the roles of resource competition and predation. We suggest here that parasitism may play a potentially important, but largely overlooked, role in the evolution of animal personalities. We identify two major routes by which parasites might influence the evolution of animal personality. First, because the risk of acquiring parasites can be influenced by an individual's behavioural type, local parasite regimes may impose selection on personality traits and behavioural syndromes (correlations between personality traits). Second, because parasite infections have consequences for aspects of host 'state', parasites might induce the evolution of individual differences in certain types of host behaviour in populations with endemic infections. Also, because infection often leads to specific changes in axes of personality, parasite infections have the potential to decouple behavioural syndromes. Host-parasite systems therefore provide researchers with valuable tools to study personality variation and behavioural syndromes from a proximate and ultimate perspective.     

The evolution of immune defense and song complexity in birds

Abstract There are three main hypotheses that explain how the evolution of parasite virulence could be linked to the evolution of secondary sexual traits, such as bird song. First, as Hamilton and Zuk proposed a role for parasites in sexual selection, female preference for healthy males in heavily parasitized species may result in extravagant trait expression. Second, a reverse causal mechanism may act, if sexual selection affects the coevolutionary dynamics of host-parasite interactions per se by selecting for increased virulence. Third, the immuno-suppressive effects of ornamentation by testosterone or limited resources may lead to increased susceptibility to parasites in species with elaborate songs. Assuming a coevolutionary relationship between parasite virulence and host investment in immune defense we used measures of immune function and song complexity to test these hypotheses in a comparative study of passerine birds. Under the first two hypotheses we predicted avian song complexity to be positively related to immune defense among species, whereas this relationship was expected to be negative if immuno-suppression was at work. We found that adult T-cell mediated immune response and the relative size of the bursa of Fabricius were independently positively correlated with a measure of song complexity, even when potentially confounding variables were held constant. Nestling T-cell response was not related to song complexity, probably reflecting age-dependent selective pressures on host immune defense. Our results are consistent with the hypotheses that predict a positive relationship between song complexity and immune function, thus indicating a role for parasites in sexual selection. Different components of the immune system may have been independently involved in this process.     

The evolution of acceptance and tolerance in hosts of avian brood parasites

Avian brood parasites lay their eggs in the nests of their hosts, which rear the parasite's progeny. The costs of parasitism have selected for the evolution of defence strategies in many host species. Most research has focused on resistance strategies, where hosts minimize the number of successful parasitism events using defences such as mobbing of adult brood parasites or rejection of parasite eggs. However, many hosts do not exhibit resistance. Here we explore why some hosts accept parasite eggs in their nests and how this is related to the virulence of the parasite. We also explore the extent to which acceptance of parasites can be explained by the evolution of tolerance; a strategy in which the host accepts the parasite but adjusts its life history or other traits to minimize the costs of parasitism. We review examples of tolerance in hosts of brood parasites (such as modifications to clutch size and multi‐broodedness), and utilize the literature on host–pathogen interactions and plant herbivory to analyse the prevalence of each type of defence (tolerance or resistance) and their evolution. We conclude that (i) the interactions between brood parasites and their hosts provide a highly tractable system for studying the evolution of tolerance, (ii) studies of host defences against brood parasites should investigate both resistance and tolerance, and (iii) tolerance and resistance can lead to contrasting evolutionary scenarios.     

Evolution of hosts paying manifold costs of defence

Hosts are expected to incur several physiological costs in defending against parasites. These include constitutive energetic (or other resource) costs of a defence system, facultative resource costs of deploying defences when parasites strike, and immunopathological costs of collateral damage. Here, we investigate the evolution of host recovery rates, varying the source and magnitude of immune costs. In line with previous work, we find that hosts paying facultative resource costs evolve faster recovery rates than hosts paying constitutive costs. However, recovery rate is more sensitive to changes in facultative costs, potentially explaining why constitutive costs are hard to detect empirically. Moreover, we find that immunopathology costs which increase with recovery rate can erode the benefits of defence, promoting chronicity of infection. Immunopathology can also lead to hosts evolving low recovery rate in response to virulent parasites. Furthermore, when immunopathology reduces fecundity as recovery rate increases (e.g. as for T-cell responses to urogenital chlamydiosis), then recovery and reproductive rates do not covary as predicted in eco-immunology. These results suggest that immunopathological and resource costs have qualitatively different effects on host evolution and that embracing the complexity of immune costs may be essential for explaining variability in immune defence in nature.     

Pollinator parasites and the evolution of floral traits

The main selective force driving floral evolution and diversity is plant–pollinator interactions. Pollinators use floral signals and indirect cues to assess flower reward, and the ensuing flower choice has major implications for plant fitness. While many pollinator behaviors have been described, the impact of parasites on pollinator foraging decisions and plant–pollinator interactions have been largely overlooked. Growing evidence of the transmission of parasites through the shared‐use of flowers by pollinators demonstrate the importance of behavioral immunity (altered behaviors that enhance parasite resistance) to pollinator health. During foraging bouts, pollinators can protect themselves against parasites through self‐medication, disease avoidance, and grooming. Recent studies have documented immune behaviors in foraging pollinators, as well as the impacts of such behaviors on flower visitation. Because pollinator parasites can affect flower choice and pollen dispersal, they may ultimately impact flower fitness. Here, we discuss how pollinator immune behaviors and floral traits may affect the presence and transmission of pollinator parasites, as well as how pollinator parasites, through these immune behaviors, can impact plant–pollinator interactions. We further discuss how pollinator immune behaviors can impact plant fitness, and how floral traits may adapt to optimize plant fitness in response to pollinator parasites. We propose future research directions to assess the role of pollinator parasites in plant–pollinator interactions and evolution, and we propose better integration of the role of pollinator parasites into research related to pollinator optimal foraging theory, floral diversity and agricultural practices.     

The Price equation framework to study disease within-host evolution

The evolution of infectious diseases is known to affect epidemiological dynamics, but, for some viruses and bacteria, this evolution also takes place inside a host during the course of an infection. I develop an original approach to study intrahost evolutionary dynamics of quantitative disease traits. This approach can be expressed mathematically using the ‘Price equation’ framework recently developed in evolutionary epidemiology. This framework combines population genetics and within-host population dynamics models to identify trade-offs that affect disease intrahost evolution and to predict short-term evolutionary dynamics of life-history traits. I show that this can be applied to study the evolution of viruses competing for host cells or to study the coevolution between parasites and the immune system of the host. This framework can also easily incorporate experimental data. Studying intrahost evolutionary dynamics provides insight at the within-host level, because it allows us to better understand the course of chronic infections, and at the epidemiological level, because it helps to study multi-scale evolutionary processes. This framework can be used to address important biological issues, from immune escape to disease evolutionary response to treatments.     

Shared control of epidemiological traits in a coevolutionary model of host-parasite interactions

Most models concerning the evolution of a parasite's virulence and its host's resistance assume that each component of the relationship (transmission, virulence, recovery, etc.) is controlled by either the host or the parasite but not by both. We present a model that describes the coevolution of host and parasite, assuming that the rate of transmission or the virulence depends on both genotypes. The evolution of these traits is constrained by trade-offs that account for costs of defense and attack strategies, in line with previous studies on the separate evolution of the host and the parasite. Considering shared control by the host and the parasite in determining the traits of the relationship leads to several novel predictions. First, the host should evolve maximal investment in defense against parasites with an intermediate replication rate. Second, the evolution of the parasite strongly depends on the way the host's defense is described. Third, the coevolutionary process may lead to decreasing the parasite's virulence as a response to a rise in the host's background mortality, contrary to classical predictions.     

Costs of an induced immune response on sexual display and longevity in field crickets

Immune system activation may benefit hosts by generating resistance to parasites. However, natural resources are usually limited, causing a trade-off between the investment in immunity and that in other life-history or sexually selected traits. Despite its importance for the evolution of host defense, state-dependent fitness costs of immunity received little attention under natural conditions. In a field experiment we manipulated the nutritional condition of male field crickets Gryllus campestris and subsequently investigated the effect of an induced immune response through inoculation of bacterial lipopolysaccharides. Immune system activation caused a condition-dependent reduction in body condition, which was proportional to the condition-gain during the preceding food-supplementation period. Independent of nutritional condition, the immune insult induced an enduring reduction in daily calling rate, whereas control-injected males fully regained their baseline level of sexual signaling following a temporary decline. Since daily calling rate affects female mate choice under natural conditions, this suggests a decline in male mating success as a cost of induced immunity. Food supplementation enhanced male life span, whereas the immune insult reduced longevity, independent of nutritional status. Thus, immune system activation ultimately curtails male fitness due to a combined decline in sexual display and life span. Our field study thus indicates a key role for fitness costs of induced immunity in the evolution of host defense. In particular, costs expressed in sexually selected traits might warrant the honest advertisement of male health status, thus representing an important mechanism in parasite-mediated sexual selection.     

Evolution of Drosophila resistance against different pathogens and infection routes entails no detectable maintenance costs

Pathogens exert a strong selective pressure on hosts, entailing host adaptation to infection. This adaptation often affects negatively other fitness‐related traits. Such trade‐offs may underlie the maintenance of genetic diversity for pathogen resistance. Trade‐offs can be tested with experimental evolution of host populations adapting to parasites, using two approaches: (1) measuring changes in immunocompetence in relaxed‐selection lines and (2) comparing life‐history traits of evolved and control lines in pathogen‐free environments. Here, we used both approaches to examine trade‐offs in Drosophila melanogaster populations evolving for over 30 generations under infection with Drosophila C Virus or the bacterium Pseudomonas entomophila, the latter through different routes. We find that resistance is maintained after up to 30 generations of relaxed selection. Moreover, no differences in several classical life‐history traits between control and evolved populations were found in pathogen‐free environments, even under stresses such as desiccation, nutrient limitation, and high densities. Hence, we did not detect any maintenance costs associated with resistance to pathogens. We hypothesize that extremely high selection pressures commonly used lead to the disproportionate expression of costs relative to their actual occurrence in natural systems. Still, the maintenance of genetic variation for pathogen resistance calls for an explanation.     

Do individual branches of immune defence correlate? A comparative case study of scavenging and non‐scavenging birds

Costs of immunity are widely believed to play an important role in life history evolution, but most studies of ecological immunology have considered only single aspects of immune function. It is unclear whether we should expect correlated responses in other aspects of immune function not measured, because individual branches of immune defence may differ in their running costs and thus may compete unequally for limiting resources, resulting in negatively correlated evolution. In theory such selection pressure may be most intense where species are hosts to more virulent parasites, thus facing a higher potential cost of parasitism. These issues are relatively unstudied, but could influence the efficacy of attempting to estimate the scale and cost of host investment in immune defence. Here, in a comparative study of birds we found that species that scavenge at carcasses, that were hypothesised to be hosts to virulent parasites, had larger spleens for their body size and higher blood total leukocyte concentrations (general measures of immune function) than non-scavengers. These results support the hypothesis that scavengers are subject to strong parasite-mediated selection on immune defences. However, measures of specific branches of immune function revealed that scavengers had a relatively lower proportion of lymphocytes than phagocytic types of leukocytes, suggesting robust front line immune defences that could potentially reduce the need for mounting relatively energetically costly lymphocyte-dependent immune responses. Following experimental inoculation, scavengers produced significantly larger humoral immune responses, but not cell-mediated immune responses, than non-scavengers. However, the sizes of cell-mediated and humoral immune responses were not correlated across species. These results suggest that single measures of immune defence may not characterise the overall immune strategy, or reveal the likely costs involved.     

Superinfection and the evolution of resistance to antimalarial drugs

A major issue in the control of malaria is the evolution of drug resistance. Ecological theory has demonstrated that pathogen superinfection and the resulting within-host competition influences the evolution of specific traits. Individuals infected with Plasmodium falciparum are consistently infected by multiple parasites; however, while this probably alters the dynamics of resistance evolution, there are few robust mathematical models examining this issue. We developed a general theory for modelling the evolution of resistance with host superinfection and examine: (i) the effect of transmission intensity on the rate of resistance evolution; (ii) the importance of different biological costs of resistance; and (iii) the best measure of the frequency of resistance. We find that within-host competition retards the ability and slows the rate at which drug-resistant parasites invade, particularly as the transmission rate increases. We also find that biological costs of resistance that reduce transmission are less important than reductions in the duration of drug-resistant infections. Lastly, we find that random sampling of the population for resistant parasites is likely to significantly underestimate the frequency of resistance. Considering superinfection in mathematical models of antimalarial drug resistance may thus be important for generating accurate predictions of interventions to contain resistance.     

Experimental evolution of resistance in Paramecium caudatum against the bacterial parasite Holospora undulata

Host-parasite coevolution is often described as a process of reciprocal adaptation and counter adaptation, driven by frequency-dependent selection. This requires that different parasite genotypes perform differently on different host genotypes. Such genotype-by-genotype interactions arise if adaptation to one host (or parasite) genotype reduces performance on others. These direct costs of adaptation can maintain genetic polymorphism and generate geographic patterns of local host or parasite adaptation. Fixation of all-resistant (or all-infective) genotypes is further prevented if adaptation trades off with other host (or parasite) life-history traits. For the host, such indirect costs of resistance refer to reduced fitness of resistant genotypes in the absence of parasites. We studied (co)evolution in experimental microcosms of several clones of the freshwater protozoan Paramecium caudatum, infected with the bacterial parasite Holospora undulata. After two and a half years of culture, inoculation of evolved and naive (never exposed to the parasite) hosts with evolved and founder parasites revealed an increase in host resistance, but not in parasite infectivity. A cross-infection experiment showed significant host clone-by-parasite isolate interactions, and evolved hosts tended to be more resistant to their own (local) parasites than to parasites from other hosts. Compared to naive clones, evolved host clones had lower division rates in the absence of the parasite. Thus, our study indicates de novo evolution of host resistance, associated with both direct and indirect costs. This illustrates how interactions with parasites can lead to the genetic divergence of initially identical populations.     

Animal personality as a cause and consequence of contest behaviour

We review the evidence for a link between consistent among-individual variation in behaviour (animal personality) and the ability to win contests over limited resources. Explorative and bold behaviours often covary with contest behaviour and outcome, although there is evidence that the structure of these ‘behavioural syndromes'' can change across situations. Aggression itself is typically repeatable, but also subject to high within-individual variation as a consequence of plastic responses to previous fight outcomes and opponent traits. Common proximate mechanisms (gene expression, endocrine control and metabolic rates) may underpin variation in both contest behaviour and general personality traits. Given the theoretical links between the evolution of fighting and of personality, we suggest that longitudinal studies of contest behaviour, combining behavioural and physiological data, would be a useful context for the study of animal personalities.     

Relative importance of chemical attractiveness to parasites for susceptibility to trematode infection

While the host immune system is often considered the most important physiological mechanism against parasites, precontact mechanisms determining exposure to parasites may also affect infection dynamics. For instance, chemical cues released by hosts can attract parasite transmission stages. We used the freshwater snail Lymnaea stagnalis and its trematode parasite Echinoparyphium aconiatum to examine the role of host chemical attractiveness, physiological condition, and immune function in determining its susceptibility to infection. We assessed host attractiveness through parasite chemo‐orientation behavior; physiological condition through host body size, food consumption, and respiration rate; and immune function through two immune parameters (phenoloxidase‐like and antibacterial activity of hemolymph) at an individual level. We found that, although snails showed high variation in chemical attractiveness to E. aconiatum cercariae, this did not determine their overall susceptibility to infection. This was because large body size increased attractiveness, but also increased metabolic activity that reduced overall susceptibility. High metabolic rate indicates fast physiological processes, including immune activity. The examined immune traits, however, showed no association with susceptibility to infection. Our results indicate that postcontact mechanisms were more likely to determine snail susceptibility to infection than variation in attractiveness to parasites. These may include localized immune responses in the target tissue of the parasite. The lack of a relationship between food consumption and attractiveness to parasites contradicts earlier findings that show food deprivation reducing snail attractiveness. This suggests that, although variation in resource level over space and time can alter infection dynamics, variation in chemical attractiveness may not contribute to parasite‐induced fitness variation within populations when individuals experience similar environmental conditions.     

Personality predicts ectoparasite abundance in an asocial sciurid

Parasitism is a consequence of complex interactions between host, parasite, and their shared environment, and host behavior can influence parasite risk. Animal personality (i.e., consistent behavioral differences that are repeatable across time and context) can influence parasitism with more explorative individuals typically hosting greater parasite loads. Host “sociality” is known to impact parasite risk with more social individuals typically at higher risk of acquiring or transmitting parasites, but other behaviors could also be important. We quantified personality in least chipmunks (Tamias minimus), including repeatability of behavioral traits, and determined whether these personality traits affected ectoparasite prevalence and abundance. We measured personality using standardized hole‐board tests and quantified ectoparasitism of 39 least chipmunks over 2 years at a site in southeastern Manitoba, Canada. We found that activity and exploration were repeatable within the context of the hole‐board test for least chipmunks, which suggests that these traits reflect personality. More exploratory individuals hosted a greater abundance of ectoparasites compared to less exploratory individuals. Our results are consistent with past studies implicating personality as a factor in host–parasite dynamics and suggest that exploration may be an important behavioral correlate of parasite acquisition.     

The evolutionary transition to coloniality promotes higher blood parasitism in birds

Parasitism has been argued as one of the major costs of breeding sociality in birds. However, there is no clear evidence for an increased parasite pressure associated with the evolutionary transition from solitary to colonial breeding. I used the pairwise comparative method to test whether colonial bird species incur in a greater risk of infection and if they must to face with a greater diversity of blood parasites (Haematozoa), by comparing pairs of congeners that included one solitary and one colonial breeding species. The richness, both in terms of number of species and number of genera, as well as the prevalence of blood parasites resulted higher in colonial species than in their solitary breeding sisters, while controlling for differences in research effort and other potentially confounding effects. These results point towards higher transmission rates of blood parasites among colonial hosts. Given the detrimental effects of blood parasites on their host fitness, the higher risk of infection and the exposition to a more diverse parasite fauna may have imposed an important cost associated to the evolution of avian coloniality. This may help to explain why colonial species have larger immune system organs, as well as to explore differences in other host life history traits potentially shaped by blood parasites.     

Spatial structure,host heterogeneity and parasite virulence: implications for vaccine‐driven evolution

Natural host‐parasite interactions exhibit considerable variation in host quality, with profound consequences for disease ecology and evolution. For instance, treatments (such as vaccination) may select for more transmissible or virulent strains. Previous theory has addressed the ecological and evolutionary impact of host heterogeneity under the assumption that hosts and parasites disperse globally. Here, we investigate the joint effects of host heterogeneity and local dispersal on the evolution of parasite life‐history traits. We first formalise a general theoretical framework combining variation in host quality and spatial structure. We then apply this model to the specific problem of parasite evolution following vaccination. We show that, depending on the type of vaccine, spatial structure may select for higher or lower virulence compared to the predictions of non‐spatial theory. We discuss the implications of our results for disease management, and their broader fundamental relevance for other causes of host heterogeneity in nature.     

Evolutionary consequence of a change in life cycle complexity: A link between precocious development and evolution toward female‐biased sex allocation in a hermaphroditic parasite

The evolutionary consequences of changes in the complex life cycles of parasites are not limited to the traits that directly affect transmission. For instance, mating systems that are altered due to precocious sexual maturation in what is typically regarded as an intermediate host may impact opportunities for outcrossing. In turn, reproductive traits may evolve to optimize sex allocation. Here, we test the hypothesis that sex allocation evolved toward a more female‐biased function in populations of the hermaphroditic digenean trematode Alloglossidium progeneticum that can precociously reproduce in their second hosts. In these precocious populations, parasites are forced to self‐fertilize as they remain encysted in their second hosts. In contrast, parasites in obligate three‐host populations have more opportunities to outcross in their third host. We found strong support that in populations with precocious development, allocation to male resources was greatly reduced. We also identified a potential phenotypically plastic response in a body size sex allocation relationship that may be driven by the competition for mates. These results emphasize how changes in life cycle patterns that alter mating systems can impact the evolution of reproductive traits in parasites.