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1. Parasite dynamics in North American monarchs predicted by host density and seasonal migratory culling

   https://doi.org/10.1111/1365-2656.13678  

   Majewska, Ania A. ; Davis, Andrew K. ; Altizer, Sonia ; de Roode, Jacobus C. ( March 2022 , Journal of Animal Ecology)

   Insect–pathogen dynamics can show seasonal and inter‐annual variations that covary with fluctuations in insect abundance and climate. Long‐term analyses are especially needed to track parasite dynamics in migratory insects, in part because their vast habitat ranges and high mobility might dampen local effects of density and climate on infection prevalence.

   Monarch butterfliesDanaus plexippusare commonly infected with the protozoanOphryocystis elektroscirrha(OE). Because this parasite lowers monarch survival and flight performance, and because migratory monarchs have experienced declines in recent decades, it is important to understand the patterns and drivers of infection.

   Here we compiled data onOEinfection spanning 50 years, from wild monarchs sampled in the United States, Canada and Mexico during summer breeding, fall migrating and overwintering periods. We examined eastern versus western North American monarchs separately, to ask how abundance estimates, resource availability, climate and breeding season length impact infection trends. We further assessed the intensity of migratory culling, which occurs when infected individuals are removed from the population during migration.

   Average infection prevalence was four times higher in western compared to eastern subpopulations. In eastern North America, the proportion of infected monarchs increased threefold since the mid‐2000s. In the western region, the proportion of infected monarchs declined sharply from 2000 to 2015, and increased thereafter. For both eastern and western subpopulations, years with greater summer adult abundance predicted greater infection prevalence, indicating that transmission increases with host breeding density. Environmental variables (temperature and NDVI) were not associated with changes in the proportion of infected adults. We found evidence for migratory culling of infected butterflies, based on declines in parasitism during fall migration. We estimated that tens of millions fewer monarchs reach overwintering sites in Mexico as a result ofOE, highlighting the need to consider the parasite as a potential threat to the monarch population.

   Increases in infection among eastern North American monarchs post‐2002 suggest that changes to the host’s ecology or environment have intensified parasite transmission. Further work is needed to examine the degree to which human practices, such as mass caterpillar rearing and the widespread planting of exotic milkweed, have contributed to this trend.

    

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2. Macroimmunology: The drivers and consequences of spatial patterns in wildlife immune defence

   https://doi.org/10.1111/1365-2656.13166  

   Becker, Daniel J. ; Albery, Gregory F. ; Kessler, Maureen K. ; Lunn, Tamika J. ; Falvo, Caylee A. ; Czirják, Gábor Á. ; Martin, Lynn B. ; Plowright, Raina K. ; Fenton, ed., Andy ( January 2020 , Journal of Animal Ecology)

   The prevalence and intensity of parasites in wild hosts varies across space and is a key determinant of infection risk in humans, domestic animals and threatened wildlife. Because the immune system serves as the primary barrier to infection, replication and transmission following exposure, we here consider the environmental drivers of immunity. Spatial variation in parasite pressure, abiotic and biotic conditions, and anthropogenic factors can all shape immunity across spatial scales. Identifying the most important spatial drivers of immunity could help pre‐empt infectious disease risks, especially in the context of how large‐scale factors such as urbanization affect defence by changing environmental conditions.

   We provide a synthesis of how to apply macroecological approaches to the study of ecoimmunology (i.e. macroimmunology). We first review spatial factors that could generate spatial variation in defence, highlighting the need for large‐scale studies that can differentiate competing environmental predictors of immunity and detailing contexts where this approach might be favoured over small‐scale experimental studies. We next conduct a systematic review of the literature to assess the frequency of spatial studies and to classify them according to taxa, immune measures, spatial replication and extent, and statistical methods.

   We review 210 ecoimmunology studies sampling multiple host populations. We show that whereas spatial approaches are relatively common, spatial replication is generally low and unlikely to provide sufficient environmental variation or power to differentiate competing spatial hypotheses. We also highlight statistical biases in macroimmunology, in that few studies characterize and account for spatial dependence statistically, potentially affecting inferences for the relationships between environmental conditions and immune defence.

   We use these findings to describe tools from geostatistics and spatial modelling that can improve inference about the associations between environmental and immunological variation. In particular, we emphasize exploratory tools that can guide spatial sampling and highlight the need for greater use of mixed‐effects models that account for spatial variability while also allowing researchers to account for both individual‐ and habitat‐level covariates.

   We finally discuss future research priorities for macroimmunology, including focusing on latitudinal gradients, range expansions and urbanization as being especially amenable to large‐scale spatial approaches. Methodologically, we highlight critical opportunities posed by assessing spatial variation in host tolerance, using metagenomics to quantify spatial variation in parasite pressure, coupling large‐scale field studies with small‐scale field experiments and longitudinal approaches, and applying statistical tools from macroecology and meta‐analysis to identify generalizable spatial patterns. Such work will facilitate scaling ecoimmunology from individual‐ to habitat‐level insights about the drivers of immune defence and help predict where environmental change may most alter infectious disease risk.

    

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3. A healthy but depleted herd: Predators decrease prey disease and density

   https://doi.org/10.1002/ecy.4063  

   Lopez, Laura K. ; Cortez, Michael H. ; DeBlieux, Turner S. ; Menel, Ilona A. ; O'Brien, Bruce ; Cáceres, Carla E. ; Hall, Spencer R. ; Duffy, Meghan A. ( May 2023 , Ecology)

   The healthy herds hypothesis proposes that predators can reduce parasite prevalence and thereby increase the density of their prey. However, evidence for such predator‐driven reductions in the prevalence of prey remains mixed. Furthermore, even less evidence supports increases in prey density during epidemics. Here, we used a planktonic predator–prey–parasite system to experimentally test the healthy herds hypothesis. We manipulated density of a predator (the phantom midge,Chaoborus punctipennis) and parasitism (the virulent fungusMetschnikowia bicuspidata) in experimental assemblages. Because we know natural populations of the prey (Daphnia dentifera) vary in susceptibility to both predator and parasite, we stocked experimental populations with nine genotypes spanning a broad range of susceptibility to both enemies. Predation significantly reduced infection prevalence, eliminating infection at the highest predation level. However, lower parasitism did not increase densities of prey; instead, prey density decreased substantially at the highest predation levels (a major density cost of healthy herds predation). This density result was predicted by a model parameterized for this system. The model specifies three conditions for predation to increase prey density during epidemics: (i) predators selectively feed on infected prey, (ii) consumed infected prey release fewer infectious propagules than unconsumed prey, and (iii) sufficiently low infection prevalence. While the system satisfied the first two conditions, prevalence remained too high to see an increase in prey density with predation. Low prey densities caused by high predation drove increases in algal resources of the prey, fueling greater reproduction, indicating that consumer–resource interactions can complicate predator–prey–parasite dynamics. Overall, in our experiment, predation reduced the prevalence of a virulent parasite but, at the highest levels, also reduced prey density. Hence, while healthy herds predation is possible under some conditions, our empirical results make it clear that the manipulation of predators to reduce parasite prevalence may harm prey density.

    

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4. Neotropical migratory and resident birds occurring in sympatry during winter have distinct haemosporidian parasite assemblages

   https://doi.org/10.1111/jbi.13760  

   Soares, Leticia ; Latta, Steven C. ; Ricklefs, Robert E. ( December 2019 , Journal of Biogeography)

   We compared the parasite assemblages of over‐wintering migratory birds and permanent residents on the wintering grounds. We determined whether parasite sharing between migratory and resident birds is influenced by host phylogenetic relatedness. We then inferred whether migratory birds transport haemosporidian parasite lineages between the breeding and wintering grounds.

   Sierra de Bahoruco National Park, Dominican Republic, Hispaniola.

   Migratory and resident birds (primarily Aves: Passeriformes) and their haemosporidian parasites (order Haemosporida,Plasmodium,HaemoproteusandParahaemoproteus).

   We used mist nets to capture birds in thorn scrub, broadleaf dry forests and pine forests during midwinter. We used molecular methods to recognize haemosporidian parasites in blood samples, and genotyped infections based on the nucleotide differences in a region of the parasite cytochromebgene.

   We identified 505 infections by 32 haemosporidian parasite lineages in 1,780 blood samples from 37 resident species, and in 901 blood samples from 14 overwintering migratory species, over five years at the same sites. Infection prevalence varied among migratory species from zero to 13%, whereas infection prevalence among resident species ranged up to 77%. Host relatedness did not predict parasite assemblage similarity. We discuss four hypotheses for the rarity of haemosporidian infections in migratory birds during winter, and for the infrequency of parasite sharing between migratory and resident birds: (a) relative abundance and host preferences of dipteran vectors lower parasite transmission to migratory birds; (b) parasite lineages adapted to infect endemic Caribbean hosts are unable to infect migratory species; (c) the physiology of migratory birds after migration and during winter reduces parasite survival; and (d) infected individuals suffer more pronounced mortality rates during migration. We highlight the link between host–parasite coevolution and the physiological adaptations associated with avian seasonal migration.

    

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5. “Resistance Is Futile”: Weaker Selection for Resistance by Abundant Parasites Increases Prevalence and Depresses Host Density

   https://doi.org/10.1086/724426  

   Walsman, Jason C. ; Duffy, Meghan A. ; Cáceres, Carla E. ; Hall, Spencer R. ( June 2023 , The American Naturalist)

   Theory often predicts that host populations should evolve greater resistance when parasites become abundant. Furthermore, that evolutionary response could ameliorate declines in host populations during epidemics. Here, we argue for an update: when all host genotypes become sufficiently infected, higher parasite abundance can select for lower resistance because its cost exceeds its benefit. We illustrate such a “resistance is futile” outcome with mathematical and empirical approaches. First, we analyzed an eco-evolutionary model of parasites, hosts, and hosts’ resources. We determined eco-evolutionary outcomes for prevalence, host density, and resistance (mathematically, “transmission rate”) along ecological and trait gradients that alter parasite abundance. With high enough parasite abundance, hosts evolve lower resistance, amplifying infection prevalence and decreasing host density. In support of these results, a higher supply of nutrients drove larger epidemics of survival-reducing fungal parasites in a mesocosm experiment. In two-genotype treatments, zooplankton hosts evolved less resistance under high-nutrient conditions than under low-nutrient conditions. Less resistance, in turn, was associated with higher infection prevalence and lower host density. Finally, in an analysis of naturally occurring epidemics, we found a broad, bimodal distribution of epidemic sizes consistent with the resistance is futile prediction of the eco-evolutionary model. Together, the model and experiment, supplemented by the field pattern, support predictions that drivers of high parasite abundance can lead to the evolution of lower resistance. Hence, under certain conditions, the most fit strategy for individual hosts exacerbates prevalence and depresses host populations. 

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