skip to main content


Title: Migration and tolerance shape host behaviour and response to parasite infection
Abstract

Numerous theoretical models have demonstrated that migration, a seasonal animal movement behaviour, can minimize the risks and costs of parasite infection. Past work on migration–infection interactions assumes migration is the only strategy available to organisms for dealing with the parasite infection, that is they migrate to a different environment to recover or escape from infection. Thus, migration is similar to the non‐spatial strategy of resistance, where hosts prevent infection or kill parasites once infected. However, an alternative defence strategy is to tolerate the infection and experience a lower cost to the infection. To our knowledge, no studies have examined how migration can change based on combining two host strategies (migration and tolerance) for dealing with parasites.

In this paper, we aim to understand how both parasite transmission and infection tolerance can influence the host's migratory behaviour.

We constructed a model that incorporates two host strategies (migration and tolerance) to understand whether allowing for tolerance affects the proportion of the population that migrates at equilibrium in response to infection.

We show that the benefits of tolerance can either decrease or increase the host's migration. Also, if the benefit of migration is great, then individuals are more likely to migrate regardless of the presence of tolerance. Finally, we find that the transmission rate of parasite infection can either decrease or increase the tolerant host's migration, depending on the cost of migration.

These findings highlight that adopting two defence strategies is not always beneficial to the hosts. Instead, a single strategy is often better, depending on the costs and benefits of the strategies and infection pressures. Our work further suggests that multiple host‐defence strategies as a potential explanation for the evolution of migration to minimize the parasite infection. Moreover, migration can also affect the ecological and evolutionary dynamics of parasite–host interactions.

 
more » « less
Award ID(s):
1654609
NSF-PAR ID:
10449928
Author(s) / Creator(s):
 ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Journal of Animal Ecology
Volume:
90
Issue:
10
ISSN:
0021-8790
Page Range / eLocation ID:
p. 2315-2324
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Species invasion and redistribution, driven by climate change and other anthropogenic influences, alter global biodiversity patterns and disrupt ecosystems. As host species move, they can bring their associated parasites with them, potentially infecting resident species, or leave their parasites behind, enhancing their competitive ability in their new ranges. General rules to predict why invading hosts will retain some parasites but not others are relatively unexplored, and the potential predictors are numerous, ranging from parasite life history to host community composition.

    In this study, we focus on the parasite retention process during host invasion. We used the Global Mammal Parasite Database to identify terrestrial mammal hosts sampled for parasites in both native and non‐native ranges. We then selected predictors likely to play a role in parasite retention, such as parasite type, parasite specialism, species composition of the invaded community, and the invading host's phylogenetic or trait‐based similarity to the new community.

    We modelled parasite retention using boosted regression trees, with a suite of 25 predictors describing parasite and host community traits. We further tested the generality of our predictions by cross‐validating models on data for other hosts and invasion locations.

    Our results show that parasite retention is nonrandom and predictable across hosts and invasions. It is broadly shaped by parasite type and parasite specialism, with more specialist parasites that infect many closely related hosts more likely to be retained. This trend is pronounced across parasite types; helminths, however, show a more uniform likelihood of retention regardless of specificity.

    Overall, we see that most parasites are not retained (11% retained), meaning many invasive species may benefit from enemy release. However, species redistribution does have the potential to spread parasites, and this also has great relevance to understanding conservation implications of species invasions. We see that specialist parasites are most likely to coinvade with their hosts, which suggests that species closely related to the invasive hosts are most likely to be affected by parasite spillover.

     
    more » « less
  2. Abstract

    Changes to migration routes and phenology create novel contact patterns among hosts and pathogens. These novel contact patterns can lead to pathogens spilling over between resident and migrant populations. Predicting the consequences of such pathogen spillover events requires understanding how pathogen evolution depends on host movement behaviour. Following spillover, pathogens may evolve changes in their transmission rate and virulence phenotypes because different strategies are favoured by resident and migrant host populations. There is conflict in current theoretical predictions about what those differences might be. Some theory predicts lower pathogen virulence and transmission rates in migrant populations because migrants have lower tolerance to infection. Other theoretical work predicts higher pathogen virulence and transmission rates in migrants because migrants have more contacts with susceptible hosts.

    We aim to understand how differences in tolerance to infection and host pace of life act together to determine the direction of pathogen evolution following pathogen spillover from a resident to a migrant population.

    We constructed a spatially implicit model in which we investigate how pathogen strategy changes following the addition of a migrant population. We investigate how differences in tolerance to infection and pace of life between residents and migrants determine the effect of spillover on pathogen evolution and host population size.

    When the paces of life of the migrant and resident hosts are equal, larger costs of infection in the migrants lead to lower pathogen transmission rate and virulence following spillover. When the tolerance to infection in migrant and resident populations is equal, faster migrant paces of life lead to increased transmission rate and virulence following spillover. However, the opposite can also occur: when the migrant population has lower tolerance to infection, faster migrant paces of life can lead to decreases in transmission rate and virulence.

    Predicting the outcomes of pathogen spillover requires accounting for both differences in tolerance to infection and pace of life between populations. It is also important to consider how movement patterns of populations affect host contact opportunities for pathogens. These results have implications for wildlife conservation, agriculture and human health.

     
    more » « less
  3. Abstract

    Most studies on the evolution of migration focus on food, mates and/or climate as factors influencing these movements, whereas negative species interactions such as predators, parasites and pathogens are often ignored. Although infection and its associated costs clearly have the potential to influence migration, thoroughly studying these interactions is challenging without a solid theoretical framework from which to develop testable predictions in natural systems.

    Here, we aim to understand when parasites favour the evolution of migration.

    We develop a general model which enables us to explore a broad range of biological conditions and to capture population and infection dynamics over both ecological and evolutionary time‐scales.

    We show that when migration evolves depends on whether the costs of migration and infection are paid in reduced fecundity or survival. Also important are the parasite transmission mode and spatiotemporal dynamics of infection and recovery (if it occurs). Finally, we find that partial migration (where only a fraction of the population migrates) can evolve but only when parasite transmission is density‐dependent.

    Our results highlight the critical, if overlooked, role of parasites in shaping long‐distance movement patterns, and suggest that infection should be considered alongside more traditional drivers of migration in both empirical and theoretical studies.

     
    more » « less
  4. Abstract

    Pathogen and parasite infections are increasingly recognized as powerful drivers of animal movement, including migration. Yet, infection‐related migration benefits can result from a combination of environmental and/or social conditions, which can be difficult to disentangle.

    Here, we focus on two infection‐related mechanisms that can favour migration: moving to escape versus recover from infection. By directly comparing the evolution of migration in response to each mechanism, we can evaluate the likely importance of changing abiotic conditions (linked to migratory recovery) with changing social conditions (linked to migratory escape) in terms of infection‐driven migration.

    We built a mathematical model and analysed it using numerically simulated adaptive dynamics to determine when migration should evolve for each migratory recovery and social migratory escape.

    We found that a higher fraction of the population migrated under migratory recovery than under social migratory escape. We also found that two distinct migratory strategies (e.g. some individuals always migrate and others only occasionally migrate) sometimes coexisted within populations with social migratory escape, but never with migratory recovery.

    Our results suggest that migratory recovery is more likely to promote the evolution of migratory behaviour, rather than escape from infected conspecifics (social migratory escape).

     
    more » « less
  5. Abstract

    Helminth parasites can have wide‐ranging, detrimental effects on host reproduction and survival. These effects are best documented in humans and domestic animals, while only a few studies in wild mammals have identified both the forces that drive helminth infection risk and their costs to individual fitness.

    Working in a well‐studied population of wild baboons (Papio cynocephalus) in the Amboseli ecosystem in Kenya, we pursued two goals, to (a) examine the costs of helminth infections in terms of female fertility and glucocorticoid hormone levels and (b) test how processes operating at multiple scales—from individual hosts to social groups and the population at large—work together to predict variation in female infection risk.

    To accomplish these goals, we measured helminth parasite burdens in 745 faecal samples collected over 5 years from 122 female baboons. We combine these data with detailed observations of host environments, social behaviours, hormone levels and interbirth intervals (IBIs).

    We found that helminths are costly to female fertility: females infected with more diverse parasite communities (i.e., higher parasite richness) exhibited longer IBIs than females infected by fewer parasite taxa. We also found that females exhibiting highTrichuris trichiuraegg counts also had high glucocorticoid levels. Female infection risk was best predicted by factors at the host, social group and population level: females facing the highest risk were old, socially isolated, living in dry conditions and infected with other helminths.

    Our results provide an unusually holistic understanding of the factors that contribute to inter‐individual differences in parasite infection, and they contribute to just a handful of studies linking helminths to host fitness in wild mammals.

     
    more » « less