Dara A. Satterfield

Loss of migratory behaviour increases infection risk for a butterfly host.

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.

Host–pathogen evolutionary signatures reveal dynamics and future invasions of vampire bat rabies

Significance In Latin America, vampire bat rabies constrains livestock production and is the main cause of lethal human rabies outbreaks. Despite knowledge that bat dispersal prevents viral extinction and compromises control campaigns, the movement patterns of infected bats are unknown. Using large host and virus datasets, we illustrate a genetic approach to link population level patterns of host dispersal to pathogen spatial spread that overcomes logistical limitations of tracking animal movement in the wild. The results implicate male vampire bats as contributing disproportionately to rabies spatial spread and offer opportunities to forecast and prevent rabies. The ubiquity of sex-biased dispersal in animals suggests sex-biased pathogen spread could widely influence the distribution and invasion dynamics of emerging diseases. 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.

Migratory monarchs wintering in California experience low infection risk compared to monarchs breeding year-round on non-native milkweed

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.

Effects of dopamine agonists on calling behavior in the green tree frog, Hyla cinerea

Dopamine (DA) is an important neurotransmitter involved in social behaviors, such as courtship and pair-bonding. In the green tree frog (Hyla cinerea), calling behavior is the primary social behavior used for mate attraction, and is critical for the reproductive success of the species. Our study examined how DA influences advertisement calling behavior of the green tree frog. In a field environment, calling males were treated with either a DA receptor-specific agonist (SKF-38393 or quinpirole), a non-specific DA agonist (apomorphine), or a control Ringers solution, and vocalizations were recorded after a 20 min post-injection period. Behavioral analyses focused on if and when the frogs called (call latency), and the number of calls produced during post-injection recordings (call rate). There were significant differences in all measurements that varied with treatment and/or dose. The results demonstrate that activation of D2-like receptors has an inhibitory effect on vocalization in the green tree frog, while the D1-like and non-specific DA agonists do not affect calling behavior. These findings coincide with behavioral data from other taxa, and support the function of D2-like receptors in the inhibition of certain social behaviors. Overall, the results suggest conservation for DA in social behaviors across vertebrates.

Variation in wing characteristics of monarch butterflies during migration: Earlier migrants have redder and more elongated wings

Abstract The migration of monarch butterflies (Danaus plexippus) in North America has a number of parallels with long-distance bird migration, including the fact that migratory populations of monarchs have larger and more elongated forewings than residents. These characteristics likely serve to optimize flight performance in monarchs, as they also do with birds. A question that has rarely been addressed thus far in birds or monarchs is if and how wing characteristics vary within a migration season. Individuals with superior flight performance should migrate quickly, and/or with minimal stopovers, and these individuals should be at the forefront of the migratory cohort. Conversely, individuals with poor flight performance and/or low endurance would be more likely to fall behind, and these would comprise the latest migrants. Here we examined how the wing morphology of migrating monarchs varies to determine if wing characteristics of early migrants differ from late migrants. We measured forewing area, elongation (length/width), and redness, which has been shown to predict flight endurance in monarchs. Based on a collection of 75 monarchs made one entire season (fall 2010), results showed that the earliest migrants (n = 20) in this cohort had significantly redder and more elongated forewings than the latest migrants (n = 17). There was also a non-significant tendency for early migrants to have larger forewing areas. These results suggest that the pace of migration in monarchs is at least partly dependent on the properties of their wings. Moreover, these data also raise a number of questions about the ultimate fate of monarchs that fall behind

Food for contagion: synthesis and future directions for studying host-parasite responses to resource shifts in anthropogenic environments

Human-provided resource subsidies for wildlife are diverse, common and have profound consequences for wildlife–pathogen interactions, as demonstrated by papers in this themed issue spanning empirical, theoretical and management perspectives from a range of study systems. Contributions cut across scales of organization, from the within-host dynamics of immune function, to population-level impacts on parasite transmission, to landscape- and regional-scale patterns of infection. In this concluding paper, we identify common threads and key findings from author contributions, including the consequences of resource subsidies for (i) host immunity; (ii) animal aggregation and contact rates; (iii) host movement and landscape-level infection patterns; and (iv) interspecific contacts and cross-species transmission. Exciting avenues for future work include studies that integrate mechanistic modelling and empirical approaches to better explore cross-scale processes, and experimental manipulations of food resources to quantify host and pathogen responses. Work is also needed to examine evolutionary responses to provisioning, and ask how diet-altered changes to the host microbiome influence infection processes. Given the massive public health and conservation implications of anthropogenic resource shifts, we end by underscoring the need for practical recommendations to manage supplemental feeding practices, limit human–wildlife conflicts over shared food resources and reduce cross-species transmission risks, including to humans. This article is part of the theme issue ‘Anthropogenic resource subsidies and host–parasite dynamics in wildlife’.

Does Skipping a Meal Matter to a Butterfly's Appearance? Effects of Larval Food Stress on Wing Morphology and Color in Monarch Butterflies

In animals with complex life cycles, all resources needed to form adult tissues are procured at the larval stage. For butterflies, the proper development of wings involves synthesizing tissue during metamorphosis based on the raw materials obtained by larvae. Similarly, manufacture of pigment for wing scales also requires resources acquired by larvae. We conducted an experiment to test the effects of food deprivation in the larval stage on multiple measures of adult wing morphology and coloration of monarch butterflies (Danaus plexippus), a species in which long-distance migration makes flight efficiency critical. In a captive setting, we restricted food (milkweed) from late-stage larvae for either 24 hrs or 48 hrs, then after metamorphosis we used image analysis methods to measure forewing surface area and elongation (length/width), which are both important for migration. We also measured the brightness of orange pigment and the intensity of black on the wing. There were correlations between several wing features, including an unexpected association between wing elongation and melanism, which will require further study to fully understand. The clearest effect of food restriction was a reduction in adult wing size in the high stress group (by approximately 2%). Patterns observed for other wing traits were ambiguous: monarchs in the low stress group (but not the high) had less elongated and paler orange pigmentation. There was no effect on wing melanism. Although some patterns obtained in this study were unclear, our results concerning wing size have direct bearing on the monarch migration. We show that if milkweed is limited for monarch larvae, their wings become stunted, which could ultimately result in lower migration success.

Responses of migratory species and their pathogens to supplemental feeding

Migratory animals undergo seasonal and often spectacular movements and perform crucial ecosystem services. In response to anthropogenic changes, including food subsidies, some migratory animals are now migrating shorter distances or halting migration altogether and forming resident populations. Recent studies suggest that shifts in migratory behaviour can alter the risk of infection for wildlife. Although migration is commonly assumed to enhance pathogen spread, for many species, migration has the opposite effect of lowering infection risk, if animals escape from habitats where pathogen stages have accumulated or if strenuous journeys cull infected hosts. Here, we summarize responses of migratory species to supplemental feeding and review modelling and empirical work that provides support for mechanisms through which resource-induced changes in migration can alter pathogen transmission. In particular, we focus on the well-studied example of monarch butterflies and their protozoan parasites in North America. We also identify areas for future research, including combining new technologies for tracking animal movements with pathogen surveillance and exploring potential evolutionary responses of hosts and pathogens to changing movement patterns. Given that many migratory animals harbour pathogens of conservation concern and zoonotic potential, studies that document ongoing shifts in migratory behaviour and infection risk are vitally needed. This article is part of the theme issue ‘Anthropogenic resource subsidies and host–parasite dynamics in wildlife’.

Patterns of parasitism in monarch butterflies during the breeding season in eastern North America

1. Migratory behaviour can result in reduced prevalence of pathogens in host populations. Two hypotheses have been proposed to explain this relationship: (i) ‘migratory escape’, where migrants benefit from escaping pathogen accumulation in contaminated environments; and (ii) ‘migratory culling’, where the selective removal of infected individuals occurs during migration.

Migratory monarchs that encounter resident monarchs show life‐history differences and higher rates of parasite infection

Environmental change induces some wildlife populations to shift from migratory to resident behaviours. Newly formed resident populations could influence the health and behaviour of remaining migrants. We investigated migrant-resident interactions among monarch butterflies and consequences for life history and parasitism. Eastern North American monarchs migrate annually to Mexico, but some now breed year-round on exotic milkweed in the southern US and experience high infection prevalence of protozoan parasites. Using stable isotopes (δ2 H, δ13 C) and cardenolide profiles to estimate natal origins, we show that migrant and resident monarchs overlap during fall and spring migration. Migrants at sites with residents were 13 times more likely to have infections and three times more likely to be reproductive (outside normal breeding season) compared to other migrants. Exotic milkweed might either attract migrants that are already infected or reproductive, or alternatively, induce these states. Increased migrant-resident interactions could affect monarch parasitism, migratory success and long-term conservation.