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Environmental change has the potential to influence trophic interactions by altering the defensive phenotype of prey. Here, we examine the effects of a pervasive environmental change driver, elevated atmospheric concentrations of CO 2 (eCO 2 ), on toxin sequestration and flight morphology of a specialist herbivore. We fed monarch butterfly larvae, Danaus plexippus , foliage from four milkweed, Asclepias , species of varying chemical defence profiles grown under either ambient or eCO 2 . We also infected a subset of these herbivores with a protozoan parasite, Ophryocystis elektroscirrha , to understand how infection and environmental change combine to alter herbivore defences. We measured changes in phytochemistry induced by eCO 2 and assessed cardenolide, toxic steroid, sequestration and wing morphology of butterflies. Monarchs compensated for lower plant cardenolide concentrations under eCO 2 by increasing cardenolide sequestration rate, maintaining similar cardenolide composition and concentrations in their wings under both CO 2 treatments. We suggest that these increases in sequestration rate are a by‐product of compensatory feeding aimed at maintaining a nutritional target in response to declining dietary quality under eCO 2 . Monarch wings were more suitable for sustained flight (more elongated) when reared on plants grown under eCO 2 or when reared on Asclepias syriaca or Asclepias incarnata rather than on Asclepias curassavica or Asclepias speciosa . Parasite infection engendered wings less suitable for sustained flight (wings became rounder) on three of four milkweed species. Wing loading (associated with powered flight) was higher on A. syriaca than on other milkweeds, whereas wing density was lower on A. curassavica . Monarchs that fed on high cardenolide milkweed developed rounder, thinner wings, which are less efficient at gliding flight. Ingesting foliage from milkweed high in cardenolides may provide protection from enemies through sequestration yet come at a cost to monarchs manifested as lower quality flight phenotypes: rounder, thinner wings with lower wing loading values. Small changes in morphology may have important consequences for enemy evasion and migration success in many animals. Energetic costs associated with alterations in defence and morphology may, therefore, have important consequences for trophic interactions in a changing world. A plain language summary is available for this article.

Understanding factors that allow highly virulent parasites to reach high infection prevalence in host populations is important for managing infection risks to human and wildlife health. Multiple transmission routes have been proposed as one mechanism by which virulent pathogens can achieve high prevalence, underscoring the need to investigate this hypothesis through an integrated modelling-empirical framework. Here, we examine a harmful specialist protozoan infecting monarch butterflies that commonly reaches high prevalence (50–100%) in resident populations. We integrate field and modelling work to show that a combination of three empirically-supported transmission routes (vertical, adult transfer and environmental transmission) can produce and sustain high infection prevalence in this system. Although horizontal transmission is necessary for parasite invasion, most new infections post-establishment arise from vertical transmission. Our study predicts that multiple transmission routes, coupled with high parasite virulence, can reduce resident host abundance by up to 50%, suggesting that the protozoan could contribute to declines of North American monarchs.

Why do parasites harm their hosts? Conventional wisdom holds that because parasites depend on their hosts for survival and transmission, they should evolve to become benign, yet many parasites cause harm. Theory predicts that parasites could evolve virulence (i.e., parasite-induced reductions in host fitness) by balancing the transmission benefits of parasite replication with the costs of host death. This idea has led researchers to predict how human interventions--such as vaccines--may alter virulence evolution, yet empirical support is critically lacking. We studied a protozoan parasite of monarch butterflies and found that higher levels of within-host replication resulted in both higher virulence and greater transmission, thus lending support to the idea that selection for parasite transmission can favor parasite genotypes that cause substantial harm. Parasite fitness was maximized at an intermediate level of parasite replication, beyond which the cost of increased host mortality outweighed the benefit of increased transmission. A separate experiment confirmed genetic relationships between parasite replication and virulence, and showed that parasite genotypes from two monarch populations caused different virulence. These results show that selection on parasite transmission can explain why parasites harm their hosts, and suggest that constraints imposed by host ecology can lead to population divergence in parasite virulence.

Apicomplexa are ancient and diverse organisms which have been poorly characterized by modern genomics. To better understand the evolution and diversity of these single-celled eukaryotes, we sequenced the genome of Ophryocystis elektroscirrha , a parasite of monarch butterflies, Danaus plexippus . We contextualize our newly generated resources within apicomplexan genomics before answering longstanding questions specific to this host-parasite system. To start, the genome is miniscule, totaling only 9 million bases and containing fewer than 3,000 genes, half the gene content of two other sequenced invertebrate-infecting apicomplexans, Porospora gigantea and Gregarina niphandrodes . We found that O. elektroscirrha shares different orthologs with each sequenced relative, suggesting the true set of universally conserved apicomplexan genes is very small indeed. Next, we show that sequencing data from other potential host butterflies can be used to diagnose infection status as well as to study diversity of parasite sequences. We recovered a similarly sized parasite genome from another butterfly, Danaus chrysippus , that was highly diverged from the O. elektroscirrha reference, possibly representing a distinct species. Using these two new genomes, we investigated potential evolutionary response by parasites to toxic phytochemicals their hosts ingest and sequester. Monarch butterflies are well-known to tolerate toxic cardenolides thanks to changes in the sequence of their Type II ATPase sodium pumps. We show that Ophryocystis completely lacks Type II or Type 4 sodium pumps, and related proteins PMCA calcium pumps show extreme sequence divergence compared to other Apicomplexa, demonstrating new avenues of research opened by genome sequencing of non-model Apicomplexa.

Pathogens are ubiquitous in insect populations and yet few studies examine their dynamics and impacts on host populations. We discuss four lepidopteran systems and explore their contributions to disease ecology and evolution. More specifically, we elucidate the role of pathogens in insect population dynamics. For three species, western tent caterpillars, African armyworm and introduced populations of gypsy moth, infection by nucleopolyhedrovirus (NPV) clearly regulates host populations or reduces their outbreaks. Transmission of NPV is largely horizontal although low levels of vertical transmission occur, and high levels of covert infection in some cases suggest that the virus can persist in a nonsymptomatic form. The prevalence of a mostly vertically transmitted protozoan parasite, Ophryocystis elektroscirrha, in monarch butterflies is intimately related to their migratory behaviour that culls highly infected individuals. Virulence and transmission are positively related among genotypes of this parasite. These systems clearly demonstrate that the interactions between insects and pathogens are highly context dependent. Not only is the outcome a consequence of changes in density and genetic diversity: environmental factors, particularly diet, can have strong impacts on virulence, transmission and host resistance or tolerance. What maintains the high level of host and pathogen diversity in these systems, however, remains a question.

The fall migration of monarch butterflies, Danaus plexippus (L.), in the Pacific Northwest was studied during 2017–2019 by tagging 14,040 captive-reared and 450 wild monarchs. One hundred and twenty-two captive-reared monarchs (0.87%) were recovered at distances averaging 899.9 ± 98.6 km for Washington-released and 630.5 ± 19.9 km for Oregon-released monarchs. The greatest straight-line release to recovery distance was 1392.1 km. A mean travel rate of 20.7 ± 2.2 km/day and maximum travel of 46.1 km/day were recorded. Recovery rates were greater for Oregon-released monarchs (0.92%) than Washington-released (0.34%) or Idaho-released monarchs (0.30%). Most monarchs (106/122) were recovered SSW-S-SSE in California, with 82 at 18 coastal overwintering sites. Two migrants from Oregon were recovered just weeks after release ovipositing in Santa Barbara and Palo Alto, CA. Two migrants released in central Washington recovered up to 360.0 km to the SE, and recoveries from Idaho releases to the S and SE suggests that some Pacific Northwest migrants fly to an alternative overwintering destination. Monarchs released in southern Oregon into smoky, poor quality air appeared to be as successful at reaching overwintering sites and apparently lived just as long as monarchs released into non-smoky, good quality air. Migration and lifespan for monarchs infected with the protozoan parasite, Ophryocystis elektroscirrha (McLaughlin and Myers), appeared to be similar to the migration and survival of uninfected monarchs, although data are limited. Our data improve our understanding of western monarch migration, serving as a basis for further studies and providing information for conservation planning.

Organisms can protect themselves against parasite-induced fitness costs through resistance or tolerance. Resistance includes mechanisms that prevent infection or limit parasite growth while tolerance alleviates the fitness costs from parasitism without limiting infection. Although tolerance and resistance affect host—parasite coevolution in fundamentally different ways, tolerance has often been ignored in animal—parasite systems. Where it has been studied, tolerance has been assumed to be a genetic mechanism, unaffected by the host environment. Here we studied the effects of host ecology on tolerance and resistance to infection by rearing monarch butterflies on 12 different species of milkweed food plants and infecting them with a naturally occurring protozoan parasite. Our results show that monarch butterflies experience different levels of tolerance to parasitism depending on the species of milkweed that they feed on, with some species providing over twofold greater tolerance than other milkweed species. Resistance was also affected by milkweed species, but there was no relationship between milkweed-conferred resistance and tolerance. Chemical analysis suggests that infected monarchs obtain highest fitness when reared on milkweeds with an intermediate concentration, diversity, and polarity of toxic secondary plant chemicals known as cardenolides. Our results demonstrate that environmental factors—such as interacting species in ecological food webs—are important drivers of disease tolerance.

Understanding host specificity and cross‐species transmission of parasites is crucial for predicting the risk and consequences of parasite spillover. We experimentally examined these dynamics in two closely related, sympatric, milkweed butterfly hosts: monarchs (Danaus plexippus) and queens (D. gilippus). The debilitating protozoan Ophryocystis elektroscirrha (OE) infects wild monarchs throughout their range, and similar neogregarine parasites have been reported from queens. We compared host resistance and tolerance to infection between hosts exposed to parasites of conspecific and heterospecific origin and examined whether differences in immune investment reflected variation in infection outcomes. Results showed that monarchs were highly susceptible to both conspecific and heterospecific parasites. In contrast, queens were susceptible almost exclusively to conspecific parasites. Queens showed greater tolerance to infection and greater immune defense in the form of melanization activity and concentration of encapsulating hemocytes. Additionally, monarch parasites caused higher pre‐adult mortality and more wing deformities than queen parasites. Given that OE can reduce monarch abundance and migratory performance, quantifying cross‐infection outcomes is important for conservation management of these two butterfly species. The greater susceptibility and costs of infection in monarchs suggest potential fitness trade‐offs against resistance and tolerance to infection in migratory hosts and underscore the need to identify factors that limit hosts' adaptation to parasites. This study explores the causes and outcomes of cross‐species parasite transmission, focusing on two congeneric and sympatric butterfly host species: monarchs (Danaus plexippus) and queens (D. gilippus), and their respective parasite strains (Ophryocystis elektroscirrha and similar parasites). Monarchs were highly susceptible to both conspecific and heterospecific parasites, whereas queens showed greater resistance, tolerance, and immune defense, underscoring the importance of quantifying cross‐infection outcomes to inform conservation strategies for these two butterfly species.

Seasonal migration occurs in many animal systems and is likely to influence interactions between animals and their parasites. Here, we focus on monarch butterflies ( Danaus plexippus ) and a protozoan parasite ( Ophryocystis elektroscirrha ) to investigate how host migration affects infectious disease processes. Previous work showed that parasite prevalence was lower among migratory than nonmigratory monarch populations; two explanations for this pattern are that (1) migration allows animals to periodically escape contaminated habitats (i.e., migratory escape), and (2) long-distance migration weeds out infected animals (i.e., migratory culling). We combined field-sampling and analysis of citizen science data to examine spatiotemporal trends of parasite prevalence and evaluate evidence for these two mechanisms. Analysis of within-breeding-season variation in eastern North America showed that parasite prevalence increased from early to late in the breeding season, consistent with the hypothesis of migratory escape. Prevalence was also positively related to monarch breeding activity, as indexed by larval density. Among adult monarchs captured at different points along the east coast fall migratory flyway, parasite prevalence declined as monarchs progressed southward, consistent with the hypothesis of migratory culling. Parasite prevalence was also lower among monarchs sampled at two overwintering sites in Mexico than among monarchs sampled during the summer breeding period. Collectively, these results indicate that seasonal migration can affect parasite transmission in wild animal populations, with implications for predicting disease risks for species with threatened migrations.

1. The emerging field of ecological immunology demonstrates that allocation by hosts to immune defence against parasites is constrained by the costs of those defences. However, the costs of non-immunological defences, which are important alternatives to canonical immune systems, are less well characterized. Estimating such costs is essential for our understanding of the ecology and evolution of alternative host defence strategies. 2. Many animals have evolved medication behaviours, whereby they use antiparasitic compounds from their environment to protect themselves or their kin from parasitism. Documenting the costs of medication behaviours is complicated by natural variation in the medicinal components of diets and their covariance with other dietary components, such as macronutrients. 3. In the current study, we explore the costs of the usage of antiparasitic compounds in monarch butterflies (Danaus plexippus), using natural variation in concentrations of antiparasitic compounds among plants. Upon infection by their specialist protozoan parasite Ophryocystis elektroscirrha, monarch butterflies can selectively oviposit on milkweed with high foliar concentrations of cardenolides, secondary chemicals that reduce parasite growth. Here, we show that these antiparasitic cardenolides can also impose significant costs on both uninfected and infected butterflies. 4. Among eight milkweed species that vary substantially in their foliar cardenolide concentration and composition, we observed the opposing effects of cardenolides on monarch fitness traits. While high foliar cardenolide concentrations increased the tolerance of monarch butterflies to infection, they reduced the survival rate of caterpillars to adulthood. Additionally, although non-polar cardenolide compounds decreased the spore load of infected butterflies, they also reduced the life span of uninfected butterflies, resulting in a hump-shaped curve between cardenolide non-polarity and the life span of infected butterflies. 5. Overall, our results suggest that the use of antiparasitic compounds carries substantial costs, which could constrain host investment in medication behaviours.