Animal migrations and parasitism: reciprocal effects within a unified framework

Migrations, i.e. the recurring, roundtrip movement of animals between distant and distinct habitats, occur among diverse metazoan taxa. Although traditionally linked to avoidance of food shortages, predators or harsh abiotic conditions, there is increasing evidence that parasites may have played a role in the evolution of migration. On the one hand, selective pressures from parasites can favour migratory strategies that allow either avoidance of infections or recovery from them. On the other hand, infected animals incur physiological costs that may limit their migratory abilities, affecting their speed, the timing of their departure or arrival, and/or their condition upon reaching their destination. During migration, reduced immunocompetence as well as exposure to different external conditions and parasite infective stages can influence infection dynamics. Here, we first explore whether parasites represent extra costs for their hosts during migration. We then review how infection dynamics and infection risk are affected by host migration, thereby considering parasites as both causes and consequences of migration. We also evaluate the comparative evidence testing the hypothesis that migratory species harbour a richer parasite fauna than their closest free-living relatives, finding general support for the hypothesis. Then we consider the implications of host migratory behaviour for parasite ecology and evolution, which have received much less attention. Parasites of migratory hosts may achieve much greater spatial dispersal than those of non-migratory hosts, expanding their geographical range, and providing more opportunities for host-switching. Exploiting migratory hosts also exerts pressures on the parasite to adapt its phenology and life-cycle duration, including the timing of major developmental, reproduction and transmission events. Natural selection may even favour parasites that manipulate their host's migratory strategy in ways that can enhance parasite transmission. Finally, we propose a simple integrated framework based on eco-evolutionary feedbacks to consider the reciprocal selection pressures acting on migratory hosts and their parasites. Host migratory strategies and parasite traits evolve in tandem, each acting on the other along two-way causal paths and feedback loops. Their likely adjustments to predicted climate change will be understood best from this coevolutionary perspective.     

Parasites hinder monarch butterfly flight: implications for disease spread in migratory hosts

Monarch butterflies (Danaus plexippus) are parasitized by the protozoan Ophryocystis elektroscirrha throughout their geographical range. Monarchs inhabiting seasonally fluctuating environments migrate annually, and parasite prevalence is lower among migratory relative to non‐migratory populations. One explanation for this pattern is that long‐distance migration weeds out infected animals, thus reducing parasite prevalence and transmission between generations. In this study we experimentally infected monarchs from a migratory population and recorded their long‐distance flight performance using a tethered flight mill. Results showed that parasitized butterflies exhibited shorter flight distances, slower flight speeds, and lost proportionately more body mass per km flown. Differences between parasitized and unparasitized monarchs were generally not explained by individual variation in wing size, shape, or wing loading, suggesting that poorer flight performance among parasitized hosts was not directly caused by morphological constraints. Effects of parasite infection on powered flight support a role for long‐distance migration in dramatically reducing parasite prevalence in this and other host–pathogen systems.     

Metabolic approaches to understanding climate change impacts on seasonal host‐macroparasite dynamics

Climate change is expected to alter the dynamics of infectious diseases around the globe. Predictive models remain elusive due to the complexity of host–parasite systems and insufficient data describing how environmental conditions affect various system components. Here, we link host–macroparasite models with the Metabolic Theory of Ecology, providing a mechanistic framework that allows integrating multiple nonlinear environmental effects to estimate parasite fitness under novel conditions. The models allow determining the fundamental thermal niche of a parasite, and thus, whether climate change leads to range contraction or may permit a range expansion. Applying the models to seasonal environments, and using an arctic nematode with an endotherm host for illustration, we show that climate warming can split a continuous spring‐to‐fall transmission season into two separate transmission seasons with altered timings. Although the models are strategic and most suitable to evaluate broad‐scale patterns of climate change impacts, close correspondence between model predictions and empirical data indicates model applicability also at the species level. As the application of Metabolic Theory considerably aids the a priori estimation of model parameters, even in data‐sparse systems, we suggest that the presented approach could provide a framework for understanding and predicting climatic impacts for many host–parasite systems worldwide.     

A long winter for the Red Queen: rethinking the evolution of seasonal migration

This paper advances an hypothesis that the primary adaptive driver of seasonal migration is maintenance of site fidelity to familiar breeding locations. We argue that seasonal migration is therefore principally an adaptation for geographic persistence when confronted with seasonality – analogous to hibernation, freeze tolerance, or other organismal adaptations to cyclically fluctuating environments. These ideas stand in contrast to traditional views that bird migration evolved as an adaptive dispersal strategy for exploiting new breeding areas and avoiding competitors. Our synthesis is supported by a large body of research on avian breeding biology that demonstrates the reproductive benefits of breeding‐site fidelity. Conceptualizing migration as an adaptation for persistence places new emphasis on understanding the evolutionary trade‐offs between migratory behaviour and other adaptations to fluctuating environments both within and across species. Seasonality‐induced departures from breeding areas, coupled with the reproductive benefits of maintaining breeding‐site fidelity, also provide a mechanism for explaining the evolution of migration that is agnostic to the geographic origin of migratory lineages (i.e. temperate or tropical). Thus, our framework reconciles much of the conflict in previous research on the historical biogeography of migratory species. Although migratory behaviour and geographic range change fluidly and rapidly in many populations, we argue that the loss of plasticity for migration via canalization is an overlooked aspect of the evolutionary dynamics of migration and helps explain the idiosyncratic distributions and migratory routes of long‐distance migrants. Our synthesis, which revolves around the insight that migratory organisms travel long distances simply to stay in the same place, provides a necessary evolutionary context for understanding historical biogeographic patterns in migratory lineages as well as the ecological dynamics of migratory connectivity between breeding and non‐breeding locations.     

Migration distance does not predict blood parasitism in a migratory songbird

Migration can influence host–parasite dynamics in animals by increasing exposure to parasites, by reducing the energy available for immune defense, or by culling of infected individuals. These mechanisms have been demonstrated in several comparative analyses; however, few studies have investigated whether conspecific variation in migration distance may also be related to infection risk. Here, we ask whether autumn migration distance, inferred from stable hydrogen isotope analysis of summer‐grown feathers (δ²H_f) in Europe, correlates with blood parasite prevalence and intensity of infection for willow warblers (Phylloscopus trochilus) wintering in Zambia. We also investigated whether infection was correlated with individual condition (assessed via corticosterone, scaled mass index, and feather quality). We found that 43% of birds were infected with Haemoproteus palloris (lineage WW1). Using generalized linear models, we found no relationship between migration distance and either Haemoproteus infection prevalence or intensity. There was spatial variation in breeding ground origins of infected versus noninfected birds, with infected birds originating from more northern sites than noninfected birds, but this difference translated into only slightly longer estimated migration distances (~214 km) for infected birds. We found no relationship between body condition indices and Haemoproteus infection prevalence or intensity. Our results do not support any of the proposed mechanisms for migration effects on host–parasite dynamics and cautiously suggest that other factors may be more important for determining individual susceptibility to disease in migratory bird species.     

Migration strategy and pathogen risk: non‐breeding distribution drives malaria prevalence in migratory waders

Pathogen exposure has been suggested as one of the factors shaping the myriad of migration strategies observed in nature. Two hypotheses relate migration strategies to pathogen infection: the ‘avoiding the tropics hypothesis’ predicts that pathogen prevalence and transmission increase with decreasing non‐breeding (wintering) latitude, while the “habitat selection hypothesis” predicts lower pathogen prevalence in marine than in freshwater habitats. We tested these scarcely investigated hypotheses by screening wintering and resident wading shorebirds (Charadriiformes) for avian malaria blood parasites (Plasmodium and Haemoproteus spp.) along a latitudinal gradient in Australia. We sequenced infections to determine if wintering migrants share malaria parasites with local shorebird residents, and we combined prevalence results with published data in a global comparative analysis. Avian malaria prevalence in Australian waders was 3.56% and some parasite lineages were shared between wintering migrants and residents, suggesting active transmission at wintering sites. In the global dataset, avian malaria prevalence was highest during winter and increased with decreasing wintering latitude, after controlling for phylogeny. The latitudinal gradient was stronger for waders that use marine and freshwater habitats (marine + freshwater) than for marine‐restricted species. Marine + freshwater wader species also showed higher overall avian malaria parasite prevalence than marine‐restricted species. By combining datasets in a global comparative analysis, we provide empirical evidence that migratory waders avoiding the tropics during the non‐breeding season experience a decreased risk of malaria parasite infection. We also find global support for the hypothesis that marine‐restricted shorebirds experience lower parasite pressures than shorebirds that also use freshwater habitats. Our study indicates that pathogen transmission may be an important driver of site selection for non‐breeding migrants, a finding that contributes new knowledge to our understanding of how migration strategies evolve.     

Evolution of spatially structured host–parasite interactions

Spatial structure has dramatic effects on the demography and the evolution of species. A large variety of theoretical models have attempted to understand how local dispersal may shape the coevolution of interacting species such as host–parasite interactions. The lack of a unifying framework is a serious impediment for anyone willing to understand current theory. Here, we review previous theoretical studies in the light of a single epidemiological model that allows us to explore the effects of both host and parasite migration rates on the evolution and coevolution of various life‐history traits. We discuss the impact of local dispersal on parasite virulence, various host defence strategies and local adaptation. Our analysis shows that evolutionary and coevolutionary outcomes crucially depend on the details of the host–parasite life cycle and on which life‐history trait is involved in the interaction. We also discuss experimental studies that support the effects of spatial structure on the evolution of host–parasite interactions. This review highlights major similarities between some theoretical results, but it also reveals an important gap between evolutionary and coevolutionary models. We discuss possible ways to bridge this gap within a more unified framework that would reconcile spatial epidemiology, evolution and coevolution.     

A synthesis of experimental work on parasite local adaptation

The study of parasite local adaptation, whereby parasites perform better on sympatric hosts than on allopatric hosts and/or better on their own host population than do other parasites, is of great importance to both basic and applied biology. Theoretical examination of host-parasite coevolution predicts that parasite migration rate, generation time and virulence all contribute to the pattern of parasite local adaptation, such that parasites with greater dispersal ability, more frequent reproduction and/or high virulence ought to exhibit increased infectivity on local hosts. Here, we present a meta-analysis of experimental work from 57 host-parasite systems across 54 local adaptation studies to directly test theoretical predictions concerning the effect of each attribute on parasite adaptation. As expected, we find that studies of parasites with higher migration rates than their hosts report local adaptation, as measured by infection success, significantly more often than studies of parasites with relatively low migration rates. Furthermore, this synthesis serves to identify biases in the current body of work and highlight areas with the greatest need for further study. We emphasize the importance of unifying the field with regard to experimental methods, local adaptation definitions and reported statistics for cross-infection studies.     

Behavioural synchronization of large‐scale animal movements – disperse alone,but migrate together?

Dispersal and migration are superficially similar large‐scale movements, but which appear to differ in terms of inter‐individual behavioural synchronization. Seasonal migration is a striking example of coordinated behaviour, enabling animal populations to track spatio‐temporal variation in ecological conditions. By contrast, for dispersal, while social context may influence an individual's emigration and settlement decisions, transience is believed to be mostly a solitary behaviour. Here, we review differences in drivers that may explain why migration appears to be more synchronized than dispersal. We derive the prediction that the contrast in the importance of behavioural synchronization between dispersal and migration is linked to differences in the selection pressures that drive their respective evolution. Although documented examples of collective dispersal are rare, this behaviour may be more common than currently believed, with important consequences for eco‐evolutionary dynamics. Crucially, to date, there is little available theory for predicting when we should expect collective dispersal to evolve, and we also lack empirical data to test predictions across species. By reviewing the state of the art in research on migration and collective movements, we identify how we can harness these advances, both in terms of theory and data collection, to broaden our understanding of synchronized dispersal and its importance in the context of global change.     

Size and accumulation of fuel reserves at stopover predict nocturnal restlessness in a migratory bird

Early arrival at the breeding site positively affects the breeding success of migratory birds. During migration, birds spend most of their time at stopovers. Therefore, determining which factors shape stopover duration is essential to our understanding of avian migration. Because the main purpose of stopover is to accumulate fat as fuel for the next flight bout, fuel reserves at arrival and the accumulation of fuel are both expected to affect stopover departure decisions. Here, we determined whether fuel reserves and fuel accumulation predict a bird''s motivation to depart, as quantified by nocturnal migratory restlessness (Zugunruhe), using northern wheatears (Oenanthe oenanthe) that were captured and temporarily contained at spring stopover. We found that fuel reserves at capture were positively correlated with Zugunruhe, and negatively correlated with fuel accumulation. This indicates that fat birds were motivated to depart, whereas lean birds were set on staying and accumulating fuel. Moreover, the change in fuel reserves was positively correlated with the concurrent change in Zugunruhe, providing the first empirical evidence for a direct link between fuel accumulation and Zugunruhe during stopover. Our study indicates that, together with innate rhythms and weather, the size and accumulation of fuel reserves shape stopover duration, and hence overall migration time.     

The strength of migratory connectivity for birds en route to breeding through the Gulf of Mexico

The strength of migratory connectivity is a measure of the cohesion of populations among phases of the annual cycle, including breeding, migration, and wintering. Many Nearctic‐Neotropical species have strong migratory connectivity between breeding and wintering phases of the annual cycle. It is less clear if this strength persists during migration when multiple endogenous and exogenous factors may decrease the cohesion of populations among routes or through time along the same routes. We sampled three bird species, American redstart Setophaga ruticilla, ovenbird Seiurus aurocapilla, and wood thrush Hylocichla mustelina, during spring migration through the Gulf of Mexico region to test if breeding populations differentiate spatially among migration routes or temporally along the same migration routes and the extent to which within‐population timing is a function of sex, age, and carry‐over from winter habitat, as measured by stable carbon isotope values in claws (δ¹³C). To make quantitative comparisons of migratory connectivity possible, we developed and used new methodology to estimate the strength of migratory connectivity (MC) from probabilistic origin assignments identified using stable hydrogen isotopes in feathers (δ²H). We found support for spatial differentiation among routes by American redstarts and ovenbirds and temporal differentiation along routes by American redstarts. After controlling for breeding origin, the timing of American redstart migration differed among ages and sexes and ovenbird migration timing was influenced by carry‐over from winter habitat. The strength of migratory connectivity did not differ among the three species, with each showing weak breeding‐to‐spring migration MC relative to prior assessments of breeding‐wintering connectivity. Our work begins to fill an essential gap in methodology and understanding of the extent to which populations remain together during migration, information critical for a full annual cycle perspective on the population dynamics and conservation of migratory animals.     

Local adaptation and the geometry of host–parasite coevolution

Metapopulation dynamics can strongly affect the ecological and evolutionary processes involved in host–parasite interactions. Here, I analyse a deterministic host–parasite coevolutionary model and derive analytic approximations for the level of local adaptation as a function of (1) host migration rate, (2) parasite migration rate, (3) parasite specificity and (4) parasite virulence. This analysis confirms the results of previous simulation studies: the difference between host and parasite migration rates may explain the level of local adaptation of both species. I also show that both higher specificity and higher virulence generally lead to higher levels of local adaptation of the species which is already ahead in the coevolutionary arms race. The present analysis also provides a simple geometric interpretation for local adaptation which captures the complexity of the temporal dynamics of host–parasite coevolution.     

A Systems Model Approach to Determining Resilience Surrogates for Case Studies

Resilience theory offers a framework for understanding the dynamics of complex systems. However, operationalizing resilience theory to develop and test empirical hypotheses can be difficult. We present a method in which simple systems models are used as a framework to identify resilience surrogates for case studies. The process of constructing a systems model for a particular case offers a path for identifying important variables related to system resilience, including the slowly-changing variables and thresholds that often are keys to understanding the resilience of a system. We develop a four-step process for identifying resilience surrogates through development of systems models. Because systems model development is often a difficult step, we summarize four basic existing systems models and give examples of how each may be used to identify resilience surrogates. The construction and analysis of simple systems models provides a useful basis for guiding and directing the selection of surrogate variables that will offer appropriate empirical measures of resilience.     

Migration costs drive convergence of threshold traits for migratory tactics

Partial migration of some, but not all, members of a population is a common form of migration. We evaluated how migration costs influence which members migrate in 10 populations of two salmonid species. The migratory patterns of both species were evaluated based on the size at maturity for resident males, which is the threshold trait that determines the migratory tactics used within a population. In both species, this size was smaller in males located further from the sea, where migration costs are presumably higher. Moreover, the threshold sizes at maturity in males were correlated between both species. Our results suggest that migration costs are a significant convergent selective force on migratory tactics and life-history traits in nature.     

How to understand species’ niches and range dynamics: a demographic research agenda for biogeography

Range dynamics causes mismatches between a species’ geographical distribution and the set of suitable environments in which population growth is positive (the Hutchinsonian niche). This is because source–sink population dynamics cause species to occupy unsuitable environments, and because environmental change creates non‐equilibrium situations in which species may be absent from suitable environments (due to migration limitation) or present in unsuitable environments that were previously suitable (due to time‐delayed extinction). Because correlative species distribution models do not account for these processes, they are likely to produce biased niche estimates and biased forecasts of future range dynamics. Recently developed dynamic range models (DRMs) overcome this problem: they statistically estimate both range dynamics and the underlying environmental response of demographic rates from species distribution data. This process‐based statistical approach qualitatively advances biogeographical analyses. Yet, the application of DRMs to a broad range of species and study systems requires substantial research efforts in statistical modelling, empirical data collection and ecological theory. Here we review current and potential contributions of these fields to a demographic understanding of niches and range dynamics. Our review serves to formulate a demographic research agenda that entails: (1) advances in incorporating process‐based models of demographic responses and range dynamics into a statistical framework, (2) systematic collection of data on temporal changes in distribution and abundance and on the response of demographic rates to environmental variation, and (3) improved theoretical understanding of the scaling of demographic rates and the dynamics of spatially coupled populations. This demographic research agenda is challenging but necessary for improved comprehension and quantification of niches and range dynamics. It also forms the basis for understanding how niches and range dynamics are shaped by evolutionary dynamics and biotic interactions. Ultimately, the demographic research agenda should lead to deeper integration of biogeography with empirical and theoretical ecology.     

Patterns and variation in the mammal parasite–glucocorticoid relationship

Parasites are ubiquitous and can strongly affect their hosts through mechanisms such as behavioural changes, increased energetic costs and/or immunomodulation. When parasites are detrimental to their hosts, they should act as physiological stressors and elicit the release of glucocorticoids. Alternatively, previously elevated glucocorticoid levels could facilitate parasite infection due to neuroimmunomodulation. However, results are equivocal, with studies showing either positive, negative or no relationship between parasite infection and glucocorticoid levels. Since factors such as parasite type, infection severity or host age and sex can influence the parasite–glucocorticoid relationship, we review the main mechanisms driving this relationship. We then perform a phylogenetic meta‐analysis of 110 records from 65 studies in mammalian hosts from experimental and observational studies to quantify the general direction of this relationship and to identify ecological and methodological drivers of the observed variability. Our review produced equivocal results concerning the direction of the relationship, but there was stronger support for a positive relationship, although causality remained unclear. Mechanisms such as host manipulation for parasite survival, host response to infection, cumulative effects of multiple stressors, and neuro‐immunomodulatory effects of glucocorticoids could explain the positive relationship. Our meta‐analysis results revealed an overall positive relationship between glucocorticoids and parasitism among both experimental and observational studies. Because all experimental studies included were parasite manipulations, we conclude that parasites caused in general an increase in glucocorticoid levels. To obtain a better understanding of the directionality of this link, experimental manipulation of glucocorticoid levels is now required to assess the causal effects of high glucocorticoid levels on parasite infection. Neither parasite type, the method used to assess parasite infection nor phylogeny influenced the relationship, and there was no evidence for publication bias. Future studies should attempt to be as comprehensive as possible, including moderators potentially influencing the parasite–glucocorticoid relationship. We particularly emphasise the importance of testing hosts of a broad age range, concomitantly measuring sex hormone levels or at least reproductive status, and for observational studies, also considering food availability, host body condition and social stressors to obtain a better understanding of the parasite–glucocorticoid relationship.     

Effects of blood parasite infections on spatiotemporal migration patterns and activity budgets in a long‐distance migratory passerine

How blood parasite infections influence the migration of hosts remains a lively debated issue as past studies found negative, positive, or no response to infections. This particularly applies to small birds, for which monitoring of detailed migration behavior over a whole annual cycle has been technically unachievable so far. Here, we investigate how bird migration is influenced by parasite infections. To this end, we tracked great reed warblers (Acrocephalus arundinaceus) with multisensor loggers, characterized general migration patterns as well as detailed flight bout durations, resting times and flight heights, and related these to the genus and intensity of their avian haemosporidian infections. We found migration distances to be shorter and the onset of autumn migration to be delayed with increasing intensity of blood parasite infection, in particular for birds with Plasmodium and mixed‐genus infections. Additionally, the durations of migratory flight bout were prolonged for infected compared to uninfected birds. But since severely infected birds and particularly birds with mixed‐genus infections had shorter resting times, initial delays seemed to be compensated for and the timing in other periods of the annual cycle was not compromised by infection. Overall, our multisensor logger approach revealed that avian blood parasites have mostly subtle effects on migratory performance and that effects can occur in specific periods of the year only.     

THE IMPACT OF SPATIAL SCALE AND HABITAT CONFIGURATION ON PATTERNS OF TRAIT VARIATION AND LOCAL ADAPTATION IN A WILD PLANT PARASITE

Theory indicates that spatial scale and habitat configuration are fundamental for coevolutionary dynamics and how diversity is maintained in host–pathogen interactions. Yet, we lack empirical data to translate the theory to natural host–parasite systems. In this study, we conduct a multiscale cross‐inoculation study using the specialist wild plant pathogen Podosphaera plantaginis on its host plant Plantago lanceolata. We apply the same sampling scheme to a region with highly fragmented (Åland) and continuous (Saaremaa) host populations. Although theory predicts higher parasite virulence in continuous regions, we did not detect differences in traits conferring virulence among the regions. Patterns of adaptation were highly scale dependent. We detected parasite maladaptation among regions, and among populations separated by intermediate distances (6.0–40.0 km) within the fragmented region. In contrast, parasite performance did not vary significantly according to host origin in the continuous landscape. For both regions, differentiation among populations was much larger for genetic variation than for phenotypic variation, indicating balancing selection maintaining phenotypic variation within populations. Our findings illustrate the critical role of spatial scale and habitat configuration in driving host–parasite coevolution. The absence of more aggressive strains in the continuous landscape, in contrast to theoretical predictions, has major implications for long‐term decision making in conservation, agriculture, and public health.     

Determinants of haemosporidian single- and co-infection risks in western palearctic birds

Understanding the drivers of infection risk helps us to detect the most at-risk species in a community and identify species whose intrinsic characteristics could act as potential reservoirs of pathogens. This knowledge is crucial if we are to predict the emergence and evolution of infectious diseases. To date, most studies have only focused on infections caused by a single parasite, leaving out co-infections. Yet, co-infections are of paramount importance in understanding the ecology and evolution of host-parasite interactions due to the wide range of effects they can have on host fitness and on the evolutionary trajectories of parasites. Here, we used a multinomial Bayesian phylogenetic modelling framework to explore the extent to which bird ecology and phylogeny impact the probability of being infected by one genus (hereafter single infection) or by multiple genera (hereafter co-infection) of haemosporidian parasites. We show that while nesting and migration behaviours influenced both the probability of being single- and co-infected, species position along the slow-fast life-history continuum and geographic range size were only pertinent in explaining variation in co-infection risk. We also found evidence for a phylogenetic conservatism regarding both single- and co-infections, indicating that phylogenetically related bird species tend to have similar infection patterns. This phylogenetic signal was four times stronger for co-infections than for single infections, suggesting that co-infections may act as a stronger selective pressure than single infections. Overall, our study underscores the combined influence of hosts’ evolutionary history and attributes in determining infection risk in avian host communities. These results also suggest that co-infection risk might be under stronger deterministic control than single infection risk, potentially paving the way toward a better understanding of the emergence and evolution of infectious diseases.