Host temperature and gut chemistry can shape resistance to parasite infection. Heat and acidity can limit trypanosomatid infection in warm-blooded hosts and could shape infection resistance in insects as well. The colony-level endothermy and acidic guts of social bees provide unique opportunities to study how temperature and acidity shape insect–parasite associations. We compared temperature and pH tolerance between three trypanosomatid parasites from social bees and a related trypanosomatid from poikilothermic mosquitoes, which have alkaline guts. Relative to the mosquito parasites, all three bee parasites had higher heat tolerance that reflected body temperatures of hosts. Heat tolerance of the honeybee parasite Crithidia mellificae was exceptional for its genus, implicating honeybee endothermy as a plausible filter of parasite establishment. The lesser heat tolerance of the emerging Lotmaria passim suggests possible spillover from a less endothermic host. Whereas both honeybee parasites tolerated the acidic pH found in bee intestines, mosquito parasites tolerated the alkaline conditions found in mosquito midguts, suggesting that both gut pH and temperature could structure host–parasite specificity. Elucidating how host temperature and gut pH affect infection—and corresponding parasite adaptations to these factors—could help explain trypanosomatids' distribution among insects and invasion of mammals.
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This content will become publicly available on January 31, 2025
Extreme heat reduces host and parasite performance in a butterfly–parasite interaction
Environmental temperature fundamentally shapes insect physiology, fitness and interactions with parasites. Differential climate warming effects on host versus parasite biology could exacerbate or inhibit parasite transmission, with far-reaching implications for pollination services, biocontrol and human health. Here, we experimentally test how controlled temperatures influence multiple components of host and parasite fitness in monarch butterflies (
- Award ID(s):
- 1659683
- NSF-PAR ID:
- 10512088
- Publisher / Repository:
- Royal Society of London
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 291
- Issue:
- 2015
- ISSN:
- 0962-8452
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Summary High temperatures (e.g., fever) and gut microbiota can both influence host resistance to infection. However, effects of temperature‐driven changes in gut microbiota on resistance to parasites remain unexplored. We examined the temperature dependence of infection and gut bacterial communities in bumble bees infected with the trypanosomatid parasite
Crithidia bombi . Infection intensity decreased by over 80% between 21 and 37°C. Temperatures of peak infection were lower than predicted based on parasite growthin vitro , consistent with mismatches in thermal performance curves of hosts, parasites and gut symbionts. Gut bacterial community size and composition exhibited slight but significant, non‐linear, and taxon‐specific responses to temperature. Abundance of total gut bacteria and of Orbaceae, both negatively correlated with infection in previous studies, were positively correlated with infection here. Prevalence of the bee pathogen‐containing family Enterobacteriaceae declined with temperature, suggesting that high temperature may confer protection against diverse gut pathogens. Our results indicate that resistance to infection reflects not only the temperature dependence of host and parasite performance, but also temperature‐dependent activity of gut bacteria. The thermal ecology of gut parasite‐symbiont interactions may be broadly relevant to infectious disease, both in ectothermic organisms that inhabit changing climates, and in endotherms that exhibit fever‐based immunity. -
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Paralechriorchis syntomentera andRibeiroia ondatrae ) with differing dispersal abilities varied in the strength of local adaptation to their amphibian hosts. Both parasites have complex life cycles involving sequential transmission among aquatic snails, larval amphibians and vertebrate definitive hosts that control dispersal across the landscape. By experimentally pairing 26 host‐by‐parasite population infection combinations from across the western USA with analyses of host and parasite spatial genetic structure, we found that increasing geographic distance—and corresponding increases in host population genetic distance—reduced infection success forP .syntomentera , which is dispersed by snake definitive hosts. For the avian‐dispersedR. ondatrae , in contrast, the geographic distance between the parasite and host populations had no influence on infection success. Differences in local adaptation corresponded to parasite genetic structure; although populations ofP .syntomentera exhibited ~10% mtDNA sequence divergence, those ofR. ondatrae were nearly identical (<0.5%), even across a 900 km range. Taken together, these results offer empirical evidence that high levels of dispersal can limit opportunities for parasites to adapt to local host populations. -
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Abstract 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.
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OE infection 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 of
OE , 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.
