Animal migrations and parasitism: reciprocal effects within a unified framework

Abstract

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.

Post COVID‐19: a solution scan of options for preventing future zoonotic epidemics

“…Other, non-taxon-specific characteristics also contribute to zoonotic pathogen risk. For example, migratory species can have a profound effect on pathogen dispersal, but these effects are complex and context dependent (Altizer, Bartel & Han, 2011;Poulin & de Angeli Dutra, 2021). Migration can play a key role in introducing disease to populations naïve to the pathogen, and the heavy toll of migration can reduce immune function, so increasing infection burden.…”

Haemosporidian taxonomic composition, network centrality and partner fidelity between resident and migratory avian hosts

“…Migration, i.e. long distance and periodical roundtrip movement of animals between distinct habitats, can alter interaction dynamics among parasites and their hosts by serving as an escape mechanism from some pathogens but also increasing parasite prevalence and richness of certain other pathogens within migrant host species (Altizer et al 2011; Satterfield et al 2015; de Angeli Dutra et al 2021a; Poulin and de Angeli Dutra 2021). Migratory behavior can also modify the availability of hosts for parasites across regions since migrant individuals do not inhabit the same habitat year-round (Bauer and Hoye 2014).…”

“…Migratory behavior can also modify the availability of hosts for parasites across regions since migrant individuals do not inhabit the same habitat year-round (Bauer and Hoye 2014). At the same time, migrants can represent an opportunity for parasites to increase their distribution worldwide, as infected migrant individuals transport their pathogens through their routes and stopovers, therefore, providing new opportunities for host switching into new environments and resident species (Altizer et al 2011; de Angeli Dutra et al 2021b; Poulin and de Angeli Dutra 2021). Indeed, the presence of migratory individuals can also affect local parasite transmission, altering parasite prevalence and richness within resident host communities (Bauer and Hoye 2014; de Angeli Dutra et al 2021b; Fecchio et al 2021).…”

“…Indeed, the presence of migratory individuals can also affect local parasite transmission, altering parasite prevalence and richness within resident host communities (Bauer and Hoye 2014; de Angeli Dutra et al 2021b; Fecchio et al 2021). However, despite the fact migration can modulate parasite-host interaction, only a few studies have addressed the implications of host migration for parasite ecology and evolution (Poulin and de Angeli Dutra 2021).…”

“…For example, for malaria parasites infecting migratory birds to be transmitted into their hosts’ new habitats, they must be able to infect and complete their cycle in new vector species under distinct environmental characteristics (Valkiūnas 2005). Hence, the exposure of parasites to abrupt environmental and vector changes may impact the ecological and evolutionary relationship between parasites and their migratory hosts since host migrations represent repeated, predictable, and directional selective pressures (Møller and Szép 2011; Poulin and de Angeli Dutra 2021). Therefore, it is essential to study how host shifts between migratory and resident hosts occurring in sympatry and under different environmental conditions can alter parasite-host dynamics.…”