Long-distance animal migrations have important consequences for infectious disease dynamics. In some cases, migration lowers pathogen transmission by removing infected individuals during strenuous journeys and allowing animals to periodically escape contaminated habitats. Human activities are now causing some migratory animals to travel shorter distances or form sedentary (non-migratory) populations. We focused on North American monarch butterflies and a specialist protozoan parasite to investigate how the loss of migratory behaviours affects pathogen spread and evolution. Each autumn, monarchs migrate from breeding grounds in the eastern US and Canada to wintering sites in central Mexico. However, some monarchs have become non-migratory and breed year-round on exotic milkweed in the southern US. We used field sampling, citizen science data and experimental inoculations to quantify infection prevalence and parasite virulence among migratory and sedentary populations. Infection prevalence was markedly higher among sedentary monarchs compared with migratory monarchs, indicating that diminished migration increases infection risk. Virulence differed among parasite strains but was similar between migratory and sedentary populations, potentially owing to high gene flow or insufficient time for evolutionary divergence. More broadly, our findings suggest that human activities that alter animal migrations can influence pathogen dynamics, with implications for wildlife conservation and future disease risks.

Anticipating how epidemics will spread across landscapes requires understanding host dispersal events that are notoriously difficult to measure. Here, we contrast host and virus genetic signatures to resolve the spatiotemporal dynamics underlying geographic expansions of vampire bat rabies virus (VBRV) in Peru. Phylogenetic analysis revealed recent viral spread between populations that, according to extreme geographic structure in maternally inherited host mitochondrial DNA, appeared completely isolated. In contrast, greater population connectivity in biparentally inherited nuclear microsatellites explained the historical limits of invasions, suggesting that dispersing male bats spread VBRV between genetically isolated female populations. Host nuclear DNA further indicated unanticipated gene flow through the Andes mountains connecting the VBRV-free Pacific coast to the VBRV-endemic Amazon rainforest. By combining Bayesian phylogeography with landscape resistance models, we projected invasion routes through northern Peru that were validated by real-time livestock rabies mortality data. The first outbreaks of VBRV on the Pacific coast of South America could occur by June 2020, which would have serious implications for agriculture, wildlife conservation, and human health. Our results show that combining host and pathogen genetic data can identify sex biases in pathogen spatial spread, which may be a widespread but underappreciated phenomenon, and demonstrate that genetic forecasting can aid preparedness for impending viral invasions.Desmodus | zoonotic disease | forecasting | sex bias | spatial dynamics

During seasonal changes around the globe, trillions of insects are on the move. Many insect populations, including butterflies, moths, hoverflies, and dragonflies, make repeated seasonal migrations each year. It is only during the past century that biologists have come to accept the concept of insect migration, and new research using radar, citizen science, and stable isotopes has revealed unexpected insights about this phenomenon. Drawing on these findings, we demonstrate how seasonal insect movements are both massive and ecologically influential, with consequences for food webs, nutrient transport, pollination, and infectious disease. Responding to environmental changes, some mobile insect populations are declining or shifting the timing and extent of their journeys. We suggest research and policy priorities for investigating and protecting insect migrations. Outcomes from such work could transform strategies for agricultural pest control and wildlife conservation, and could help preserve the ecological functions performed by migratory insects.

Long-distance migration can lower infection risk for animal populations by removing infected individuals during strenuous journeys, spatially separating susceptible age classes, or allowing migrants to periodically escape from contaminated habitats. Many seasonal migrations are changing due to human activities including climate change and habitat alteration. Moreover, for some migratory populations, sedentary behaviors are becoming more common as migrants abandon or shorten their journeys in response to supplemental feeding or warming temperatures. Exploring the consequences of reduced movement for host-parasite interactions is needed to predict future responses of animal pathogens to anthropogenic change. Monarch butterflies (Danaus plexippus) and their specialist protozoan parasite Ophryocystis elektroscirrha (OE) provide a model system for examining how long-distance migration affects infectious disease processes in a rapidly changing world. Annual monarch migration from eastern North America to Mexico is known to reduce protozoan infection prevalence, and more recent work suggests that monarchs that forego migration to breed year-round on non-native milkweeds in the southeastern and south central Unites States face extremely high risk of infection. Here, we examined the prevalence of OE infection from 2013 to 2016 in western North America, and compared monarchs exhibiting migratory behavior (overwintering annually along the California coast) with those that exhibit year-round breeding. Data from field collections and a joint citizen science program of Monarch Health and Monarch Alert showed that infection frequency was over nine times higher for monarchs sampled in gardens with year-round milkweed as compared to migratory monarchs sampled at overwintering sites. Results here underscore the importance of animal migrations for lowering infection risk and motivate future studies of pathogen transmission in migratory species affected by environmental change.