Host Developmental Stage Effects on Parasite Resistance and Tolerance.

AbstractHosts can defend themselves against parasites either by preventing or limiting infections (resistance) or by limiting parasite-induced damage (tolerance). However, it remains underexplored how these defense types vary over host development with shifting patterns of resource allocation priorities. Here, we studied the role played by developmental stage in resistance and tolerance in Atlantic salmon (Salmo salar). This anadromous fish has distinct life stages related to living in freshwater and seawater. We experimentally exposed 1-year-old salmon, either at the freshwater stage or at the stage transitioning to the marine phase, to the trematode Diplostomum pseudospathaceum. Using 56 pedigreed families and multivariate animal models, we show that developmental transition is associated with reduced resistance but does not affect tolerance. Furthermore, by comparing tolerance slopes (host fitness against parasite load) based on additive genetic effects among infected and unexposed control relatives, we observed that the slopes can be largely independent of the infection, that is, they may not reflect tolerance. Together, our results suggest that the relative importance of different defense types may vary with host development and emphasize the importance of including control treatments for more confident interpretations of tolerance estimates.

Life-history genotype explains variation in migration activity in Atlantic salmon (Salmo salar).

One of the most well-known life-history continuums is the fast-slow axis, where 'fast' individuals mature earlier than 'slow' individuals. 'Fast' individuals are predicted to be more active than 'slow' individuals because high activity is required to maintain a fast life-history strategy. Recent meta-analyses revealed mixed evidence for such integration. Here, we test whether known life-history genotypes differ in activity expression by using Atlantic salmon (Salmo salar) as a model. In salmon, variation in Vgll3, a transcription cofactor, explains approximately 40% of variation in maturation timing. We predicted that the allele related to early maturation (vgll3*E) would be associated with higher activity. We used an automated surveillance system to follow approximately 1900 juveniles including both migrants and non-migrants (i.e. smolt and parr fish, respectively) in semi-natural conditions over 31 days (approx. 580 000 activity measurements). In migrants, but not in non-migrants, vgll3 explained variation in activity according to our prediction in a sex-dependent manner. Specifically, in females the vgll3*E allele was related to increasing activity, whereas in males the vgll3*L allele (later maturation allele) was related to increasing activity. These sex-dependent effects might be a mechanism maintaining within-population genetic life-history variation.

Cold water reduces the severity of parasite-inflicted damage: support for wintertime recuperation in aquatic hosts.

The reduction in host fitness caused by parasite infections (virulence) depends on infection intensity and the degree of damage caused per parasite. Environmental conditions can shape both virulence components, but in contrast to infection intensity, environmental impacts on per-parasite damage are poorly understood. Here, we studied the effect of ambient temperature on per-parasite damage, which is jointly determined by the ability of parasites to induce harm (per-parasite pathogenicity) and the ability of hosts to limit damage (tolerance). We experimentally exposed two salmonid species, Atlantic salmon (Salmo salar) and sea trout (Salmo trutta), to replicated genotypes of the eye fluke Diplostomum pseudospathaceum. After development of health damage (eye cataracts) in warm water (16 °C) during the first 12 weeks post exposure, we maintained the fish at either 5 °C (cold water) or 16 °C for another 8 weeks and quantified changes in cataracts as a function of parasite load. We found that per-parasite damage was reduced in cold compared to warm water, suggesting that cold temperatures improved host health. Per-parasite damage was also affected by parasite genotype and host species, but these effects did not change with temperature. Our findings suggest that cold-water seasons, which are often neglected in host-parasite studies due to low infection risk, could allow hosts to recuperate and thus, may have important implications for the ecology and epidemiology of parasite infections.

Negative associations between parasite avoidance, resistance and tolerance predict host health in salmonid fish populations.

Genetic variation in defence against parasite infections is fundamental for host-parasite evolution. The overall level of defence of a host individual or population includes mechanisms that reduce parasite exposure (avoidance), establishment (resistance) or pathogenicity (tolerance). However, how these traits operate and evolve in concert is not well understood. Here, we investigated genetic variation in and associations between avoidance, resistance and tolerance in a natural host-parasite system. Replicated populations of Atlantic salmon (Salmo salar) and sea trout (an anadromous form of brown trout, Salmo trutta) were raised under common garden conditions and infected with the eye fluke Diplostomum pseudospathaceum. We demonstrate significant genetic variation in the defence traits across host populations and negative associations between the traits, with the most resistant populations showing the weakest avoidance and the lowest infection tolerance. These results are suggestive of trade-offs between different components of defence and possibly underlie the genetic variation in defence traits observed in the wild. Because the three defence mechanisms affect host-parasite evolution in profoundly different ways, we emphasize the importance of studying these traits in concert.

Within-host interactions shape virulence-related traits of trematode genotypes.

Within-host interactions between co-infecting parasites can significantly influence the evolution of key parasite traits, such as virulence (pathogenicity of infection). The type of interaction is expected to predict the direction of selection, with antagonistic interactions favouring more virulent genotypes and synergistic interactions less virulent genotypes. Recently, it has been suggested that virulence can further be affected by the genetic identity of co-infecting partners (G × G interactions), complicating predictions on disease dynamics. Here, we used a natural host-parasite system including a fish host and a trematode parasite to study the effects of G × G interactions on infection virulence. We exposed rainbow trout (Oncorhynchus mykiss) either to single genotypes or to mixtures of two genotypes of the eye fluke Diplostomum pseudospathaceum and estimated parasite infectivity (linearly related to pathogenicity of infection, measured as coverage of eye cataracts) and relative cataract coverage (controlled for infectivity). We found that both traits were associated with complex G × G interactions, including both increases and decreases from single infection to co-infection, depending on the genotype combination. In particular, combinations where both genotypes had low average infectivity and relative cataract coverage in single infections benefited from co-infection, while the pattern was opposite for genotypes with higher performance. Together, our results show that infection outcomes vary considerably between single and co-infections and with the genetic identity of the co-infecting parasites. This can result in variation in parasite fitness and consequently impact evolutionary dynamics of host-parasite interactions.

Learned parasite avoidance is driven by host personality and resistance to infection in a fish-trematode interaction.

Cognitive abilities related to the assessment of risk improve survival. While earlier studies have examined the ability of animals to learn to avoid predators, learned parasite avoidance has received little interest. In a series of behavioural trials with the trematode parasite Diplostomum pseudospathaceum, we asked whether sea trout (Salmo trutta trutta) hosts show associative learning in the context of parasitism and if so, whether learning capacity is related to the likelihood of infection mediated through host personality and resistance. We show that animals are capable of learning to avoid visual cues associated with the presence of parasites. However, avoidance behaviour ceased after the likely activation of host resistance following consecutive exposures during learning, suggesting that resistance to infection outweighs avoidance. Further, we found a positive relationship between learning ability and boldness, suggesting a compensation of risky lifestyles through increased investment in cognitive abilities. By contrast, an increased risk of infection due to low resistance was not balanced by learning ability. Instead, these traits were positively related, which may be explained by inherent physiological qualities controlling both traits. Overall, the results demonstrate that parasitism, in addition to other biological interactions such as predation, is an important selective factor in the evolution of animal cognition.

Host infection history modifies co-infection success of multiple parasite genotypes.

Co-infections by multiple parasite genotypes are common and have important implications for host-parasite ecology and evolution through within-host interactions. Typically, these infections take place sequentially, and therefore, the outcome of co-infection may be shaped by host immune responses triggered by previous infections. For example, in vertebrates, specific immune responses play a central role in protection against disease over the course of life, but co-infection research has mostly focused on previously uninfected individuals. Here, we investigated whether sequential exposure and activation of host resistance in rainbow trout Oncorhynchus mykiss affects infection success and interactions between co-infecting parasite genotypes of the trematode eye-fluke Diplostomum pseudospathaceum. In accordance with earlier results, we show that a simultaneous attack of two parasite genotypes facilitates parasite establishment in previously uninfected hosts. However, we find for the first time that this facilitation in co-infection is lost in hosts with prior infection. We conclude that vertebrate host infection history can affect the direction of within-host-parasite interactions. Our results may have significant implications for the evolution of co-infections and parasite transmission strategies.

Contrasting effects of large density changes on relative testes size in fluctuating populations of sympatric vole species.

Across species, there is usually a positive relationship between sperm competition level and male reproductive effort on ejaculates, typically measured using relative testes size (RTS). Within populations, demographic and ecological processes may drastically alter the level of sperm competition and thus, potentially affect the evolution of testes size. Here, we use longitudinal records (across 38 years) from wild sympatric Fennoscandian populations of five species of voles to investigate whether RTS responds to natural fluctuations in population density, i.e. variation in sperm competition risk. We show that for some species RTS increases with density. However, our results also show that this relationship can be reversed in populations with large-scale between-year differences in density. Multiple mechanisms are suggested to explain the negative RTS-density relationship, including testes size response to density-dependent species interactions, an evolutionary response to sperm competition levels that is lagged when density fluctuations are over a certain threshold, or differing investment in pre- and post-copulatory competition at different densities. The results emphasize that our understanding of sperm competition in fluctuating environments is still very limited.

Quantity and Quality of Aquaculture Enrichments Influence Disease Epidemics and Provide Ecological Alternatives to Antibiotics.

Environmental heterogeneity is a central component influencing the virulence and epidemiology of infectious diseases. The number and distribution of susceptible hosts determines disease transmission opportunities, shifting the epidemiological threshold between the spread and fadeout of a disease. Similarly, the presence and diversity of other hosts, pathogens and environmental microbes, may inhibit or accelerate an epidemic. This has important applied implications in farming environments, where high numbers of susceptible hosts are maintained in conditions of minimal environmental heterogeneity. We investigated how the quantity and quality of aquaculture enrichments (few vs. many stones; clean stones vs. stones conditioned in lake water) influenced the severity of infection of a pathogenic bacterium, Flavobacterium columnare, in salmonid fishes. We found that the conditioning of the stones significantly increased host survival in rearing tanks with few stones. A similar effect of increased host survival was also observed with a higher number of unconditioned stones. These results suggest that a simple increase in the heterogeneity of aquaculture environment can significantly reduce the impact of diseases, most likely operating through a reduction in pathogen transmission (stone quantity) and the formation of beneficial microbial communities (stone quality). This supports enriched rearing as an ecological and economic way to prevent bacterial infections with the minimal use of antimicrobials.

Polyandry enhances offspring survival in an infanticidal species.

The adaptive significance of polyandry is an intensely debated subject in sexual selection. For species with male infanticidal behaviour, it has been hypothesized that polyandry evolved as female counterstrategy to offspring loss: by mating with multiple males, females may conceal paternity and so prevent males from killing putative offspring. Here we present, to our knowledge, the first empirical test of this hypothesis in a combined laboratory and field study, and show that multiple mating seems to reduce the risk of infanticide in female bank voles Myodes glareolus. Our findings thus indicate that females of species with non-resource based mating systems, in which males provide nothing but sperm, but commit infanticide, can gain non-genetic fitness benefits from polyandry.

Long-term fitness benefits of polyandry in a small mammal, the bank vole Clethrionomys glareolus.

Polyandry, i.e. mating with multiple males within one reproductive event, is a common female mating strategy but its adaptive function is often unclear. We tested whether polyandrous females gain genetic benefits by comparing fitness traits of monandrous (mated twice with a single male) and polyandrous (mated twice with two different males) female bank voles Clethrionomys glareolus. We raised the offspring in the laboratory until adulthood and measured their body size, before releasing them to outdoor enclosures to overwinter. At the onset of the breeding season in the following spring, we found that offspring of polyandrous females performed significantly better at reproduction than those of monandrous females. This was mainly due to sons of polyandrous females producing significantly more offspring than those of monandrous females. No significant differences were found for offspring body mass or winter survival between the two treatments. Our results appear to provide evidence that bank vole females gain long-term benefits from polyandry.

Vertebrate defense against parasites: Interactions between avoidance, resistance, and tolerance.

Hosts can utilize different types of defense against the effects of parasitism, including avoidance, resistance, and tolerance. Typically, there is tremendous heterogeneity among hosts in these defense mechanisms that may be rooted in the costs associated with defense and lead to trade-offs with other life-history traits. Trade-offs may also exist between the defense mechanisms, but the relationships between avoidance, resistance, and tolerance have rarely been studied. Here, we assessed these three defense traits under common garden conditions in a natural host-parasite system, the trematode eye-fluke Diplostomum pseudospathaceum and its second intermediate fish host. We looked at host individuals originating from four genetically distinct populations of two closely related salmonid species (Atlantic salmon, Salmo salar and sea trout, Salmo trutta trutta) to estimate the magnitude of variation in these defense traits and the relationships among them. We show species-specific variation in resistance and tolerance and population-specific variation in resistance. Further, we demonstrate evidence for a trade-off between resistance and tolerance. Our results suggest that the variation in host defense can at least partly result from a compromise between different interacting defense traits, the relative importance of which is likely to be shaped by environmental components. Overall, this study emphasizes the importance of considering different components of the host defense system when making predictions on the outcome of host-parasite interactions.

Population sex-ratio affecting behavior and physiology of overwintering bank voles (Myodes glareolus).

Many boreal rodents are territorial during the breeding season but during winter become social and aggregate for more energy efficient thermoregulation. Communal winter nesting and social interactions are considered to play an important role for the winter survival of these species, yet the topic is relatively little explored. Females are suggested to be the initiators of winter aggregations and sometimes reported to survive better than males. This could be due to the higher social tolerance observed in overwintering females than males. Hormonal status could also affect winter behavior and survival. For instance, chronic stress can have a negative effect on survival, whereas high gonadal hormone levels, such as testosterone, often induce aggressive behavior. To test if the winter survival of females in a boreal rodent is better than that of males, and to assess the role of females in the winter aggregations, we generated bank vole (Myodes glareolus) populations of three different sex ratios (male-biased, female-biased and even density) under semi-natural conditions. We monitored survival, spatial behavior and hormonal status (stress and testosterone) during two winter months. We observed no significant differences in survival between the sexes or among populations with differing sex-ratios. The degree of movement area overlap was used as an indicator of social tolerance and potential communal nesting. Individuals in male biased populations showed a tendency to be solitary, whereas in female biased populations there was an indication of winter aggregation. Females living in male-biased populations had higher stress levels than the females from the other populations. The female-biased sex-ratio induced winter breeding and elevated testosterone levels in males. Thus, our results suggest that the sex-ratio of the overwintering population can lead to divergent overwintering strategies in bank voles.

Strategic adjustments in sperm production within and between two island populations of house mice.

Sperm production is physiologically costly. Consequently, males are expected to be prudent in their sperm production, and tailor their expenditure according to prevailing social conditions. Differences in sperm production have been found across island populations of house mice that differ in the level of selection from sperm competition. Here, we determined the extent to which these differences represent phenotypic plasticity and/or population divergence in sperm production. We sourced individuals from two populations at the extreme levels of sperm competition, and raised them under common-garden conditions while manipulating the social experience of developing males. Males from the high-sperm competition population produced more sperm and better quality sperm than did males from the low-sperm competition population. In addition, males reared under a perceived "risk" of sperm competition produced greater numbers of sperm than males reared with "no risk." However, our analyses revealed that phenotypic plasticity in sperm production was greater for individuals from the high-sperm competition population. Our results are thus consistent with both population divergence and phenotypic plasticity in sperm production, and suggest that population level of sperm competition might affect the degree of adaptive plasticity in sperm production in response to sperm competition risk.

Variation in predation risk and vole feeding behaviour: a field test of the risk allocation hypothesis.

Many prey animals experience temporal variation in the risk of predation and therefore face the problem of allocating their time between antipredator efforts and other activities like feeding and breeding. We investigated time allocation of prey animals that balanced predation risk and feeding opportunities. The predation risk allocation hypothesis predicts that animals should forage more in low- than in high-risk situations and that this difference should increase with an increasing attack ratio (i.e. difference between low- and high-risk situations) and proportion of time spent at high risk. To test these predictions we conducted a field test using bank voles ( Clethrionomys glareolus) as a prey and the least weasel ( Mustela nivalis nivalis) as a predator. The temporal pattern and intensity of predation risk were manipulated in large outdoor enclosures and the foraging effort and patch use of voles were measured by recording giving-up densities. We did not observe any variation in feeding effort due to changes in the level of risk or the proportion of time spent under high-risk conditions. The only significant effect was found when the attack ratio was altered: the foraging effort of voles was higher in the treatment with a low attack ratio than in the treatment with a high attack ratio. Thus the results did not support the predation risk allocation hypothesis and we question the applicability of the hypothesis to our study system. We argue that the deviation between the observed pattern of feeding behaviour of bank voles and that predicted by the predation risk allocation hypothesis was mostly due to the inability of voles to accurately assess the changes in the level of risk. However, we also emphasise the difficulties of testing hypotheses under outdoor conditions and with mammals capable of flexible behavioural patterns.