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1. “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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2. Parasite exposure and host susceptibility jointly drive the emergence of epidemics

   https://doi.org/10.1002/ecy.3245  

   Stewart Merrill, Tara E. ; Hall, Spencer R. ; Cáceres, Carla E. ( December 2020 , Ecology)

   Parasite transmission is thought to depend on both parasite exposure and host susceptibility to infection; however, the relative contribution of these two factors to epidemics remains unclear. We used interactions between an aquatic host and its fungal parasite to evaluate how parasite exposure and host susceptibility interact to drive epidemics. In six lakes, we tracked the following factors from pre‐epidemic to epidemic emergence: (1) parasite exposure (measured observationally as fungal spores attacking wild‐caught hosts), (2) host susceptibility (measured experimentally as the number of fungal spores required to produce terminal infection), (3) host susceptibility traits (barrier resistance and internal clearance, both quantified with experimental assays), and (4) parasite prevalence (measured observationally from wild‐caught hosts). Tracking these factors over 6 months and in almost 7,000 wild‐caught hosts provided key information on the drivers of epidemics. We found that epidemics depended critically on the interaction of exposure and susceptibility; epidemics only emerged when a host population’s level of exposure exceeded its individuals’ capacity for recovery. Additionally, we found that host internal clearance traits (the hemocyte response) were critical in regulating epidemics. Our study provides an empirical demonstration of how parasite exposure and host susceptibility interact to inhibit or drive disease in natural systems and demonstrates that epidemics can be delayed by asynchronicity in the two processes. Finally, our results highlight how individual host traits can scale up to influence broad epidemiological patterns.

    

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3. Impact of the acanthocephalan parasite Profilicollis altmani on the fecundity of its crustacean intermediate host, the Pacific mole crab, Emerita analoga

   https://doi.org/10.1111/ivb.12362  

   Bhaduri, Ritindra N. ; Yamaguchi, Taiga J. ; Munguia, Kimberly ; Sandhu, Royal K. ; Coffey, Victoria R. ( January 2022 , Invertebrate Biology)

   Parasites may influence their hosts in multiple ways, ranging from physiological changes and behavioral modifications, to altering life history traits. One fitness component that is often considered in relation to parasitism is host fecundity. The larval acanthocephalan parasite,Profilicollis altmani, commonly infects the Pacific mole crab,Emerita analoga; yet this parasite's effect on the crab's fecundity is unknown. Consequently, we examined the effects of acanthocephalan parasitism on the fecundity of this mole crab species. Crabs were collected from the swash intertidal zone in Monterey Bay, CA, and the following parameters were quantified: crab body size (carapace length) and weight, egg‐bearing status (nongravid and gravid), egg number and diameter, total volume and weight of egg mass, and their developmental stages (from newly laid eggs to recognizable zoea larval stage). Parasite prevalence, intensity of infection, and body size of larval cystacanths (measured as volume) were assessed. Host fecundity was positively correlated with both body size and body weight. No differences in egg weight were found between uninfected and infected crabs. Similarly, no difference in crab body weight at various embryonic developmental phases was documented between uninfected and infected crabs. Cystacanth volumes in infected nongravid and infected gravid crabs were not significantly different. Our study suggests that the parasiteP. altmanidoes not have any appreciable effect on the fecundity ofE. analogaand that female mole crabs undergo normal reproduction and maintain robust population sizes in their natural environments. Our findings thus appear to moderate the pervasive notion of a major impact of parasitism on host reproduction.

    

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4. Experimental habitat fragmentation disrupts host–parasite interaction over decades via life‐cycle bottlenecks

   https://doi.org/10.1002/ecy.3758  

   Bitters, Matthew E. ; Meyers, Jacqui ; Resasco, Julian ; Sarre, Stephen D. ; Tuff, Kika T. ; Davies, Kendi F. ( June 2022 , Ecology)

   Habitat loss and fragmentation are likely to seriously impact parasites, a less studied but critical component of ecosystems, yet we lack long‐term experimental evidence. Parasites structure communities, increase connectivity in food webs, and account for a large proportion of an ecosystem's total biomass. Food web models predict that parasites with multiple obligate hosts are at greater risk of extinction because the local extinction, or reduction in abundance, of any host will result in a life‐cycle bottleneck for the parasite. We examine the response of a parasite and its multiple hosts to forest fragmentation over 26 years in the Wog Wog Habitat Fragmentation Experiment in southeastern Australia. The parasite is the nematodeHedruris wogwogensis, its intermediate host is the amphipod,Arcitalitrus sylvaticus, and its definitive host is the skink,Lampropholis guichenoti. In the first decade after fragmentation, nematodes completely disappeared from the matrix (plantation forestry) and all but disappeared from their definitive host (skinks) in fragments, and by the third decade after fragmentation had not appreciably recovered anywhere in the fragmented landscape compared to continuous forest. The low prevalence of the nematode in the fragmented landscape was associated with the low abundance of one or the other host in different decades: low abundance of the intermediate host (amphipod) in the first decade and low abundance of the definitive host (skink) in the third decade. In turn, the low abundance of each host was associated with changes to the abiotic environment over time due largely to the dynamically changing matrix as the plantation trees grew. Our study provides rare long‐term experimental evidence of how disturbance can cause local extinction in parasites with life cycles dependent on more than one host species through population bottlenecks at any life stage. Mismatches in the abundance of multiple hosts over time are likely to be common following disturbance, thus causing parasites with complex life cycles to be particularly susceptible to habitat fragmentation and other disturbances. The integrity of food webs, communities, and ecosystems in fragmented landscapes may be more compromised than presently appreciated due to the sensitivity of parasites to habitat fragmentation.

    

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5. 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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