Infection with the trypanosome Crithidia bombi and expression of immune-related genes in the bumblebee Bombus terrestris

The immune system is a general mechanism that reduces the fitness cost of parasitism. In this study, we examined variation in immune responses under natural conditions in the bumblebee Bombus terrestris. Using 14 colonies reared in the field, we compared the immune response to an artificial implant between workers that could or could not forage (86 control and 91 nonforaging workers). Foraging activity was prevented by cutting a large part of the wings. As expected, control workers had lower immune responses than nonforaging workers in 10 of 14 colonies. Overall, the treatment effect was significant even though weak, suggestive of a trade-off between immune defence and foraging activity. We also examined the environmental factors that might covary with the immune response in workers. The immune response significantly decreased in workers that were naturally infected by the intestinal parasite Crithidia bombi and increased with a measure of colony success, the maximum number of workers. These correlations suggest that the strength of immune responses reflects individual, and hence colony condition.

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Single-clone and mixed-clone infections versus host environment in Crithidia bombi infecting bumblebees

Parasitology ◽

10.1017/s0031182098003138 ◽

1998 ◽

Vol 117 (4) ◽

pp. 331-336 ◽

Cited By ~ 37

Author(s):

B. IMHOOF ◽

P. SCHMID-HEMPEL

Keyword(s):

Bombus Terrestris ◽

Infection Intensity ◽

Parasite Prevalence ◽

Mixed Genotype ◽

Host Environment ◽

Crithidia Bombi ◽

The Family ◽

Single Clone ◽

Parasite Evolution ◽

Host Heterogeneity

Current theories assume that adaptive parasite evolution explains variation in the level of virulence and parasite success. In particular, mixed-genotype infections by parasites should generally be more virulent, and faster multiplying strains more successful, either because fixed strategies have evolved or because parasites facultatively alter virulence in response to co-infecting competitors. We compared several measures of parasite success and virulence between single-clone and mixed-clone infections of 2 strains of the trypanosome Crithidia bombi in its bumblebee host, Bombus terrestris. Contrary to expectation, we could not find differences between single-clone and mixed-clone infections in parasite prevalence, infection success, duration and clearance rate. However, a clearly significant effect of colony on infection intensity was present, and the colony effect emerged in virtually all other measures. We thus conclude that host environment as defined by the family (colony) genotype and thus host heterogeneity are more important in determining parasite virulence than the parasite characteristics. This does not invalidate modern theories of parasite evolution but suggests that variation in both hosts and parasites must be taken into account in more detail.

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Effects of natal and novel Crithidia bombi (Trypanosomatidae) infections on Bombus terrestris hosts

Insectes Sociaux ◽

10.1007/s00040-007-0974-1 ◽

2007 ◽

Vol 55 (1) ◽

pp. 86-90 ◽

Cited By ~ 19

Author(s):

C. P. Yourth ◽

M. J. F. Brown ◽

P. Schmid-Hempel

Keyword(s):

Bombus Terrestris ◽

Crithidia Bombi

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Insect antimicrobial peptides act synergistically to inhibit a trypanosome parasite

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2015.0302 ◽

2016 ◽

Vol 371 (1695) ◽

pp. 20150302 ◽

Cited By ~ 28

Author(s):

Monika Marxer ◽

Vera Vollenweider ◽

Paul Schmid-Hempel

Keyword(s):

Antimicrobial Peptides ◽

Evolutionary Ecology ◽

Bombus Terrestris ◽

Parasite Strain ◽

Strain Specificity ◽

Variable Expression ◽

Combination Treatments ◽

Crithidia Bombi ◽

Spectrum Activity ◽

Different Strains

The innate immune system provides protection from infection by producing essential effector molecules, such as antimicrobial peptides (AMPs) that possess broad-spectrum activity. This is also the case for bumblebees, Bombus terrestris , when infected by the trypanosome, Crithidia bombi . Furthermore, the expressed mixture of AMPs varies with host genetic background and infecting parasite strain (genotype). Here, we used the fact that clones of C. bombi can be cultivated and kept as strains in medium to test the effect of various combinations of AMPs on the growth rate of the parasite. In particular, we used pairwise combinations and a range of physiological concentrations of three AMPs, namely Abaecin , Defensin and Hymenoptaecin , synthetized from the respective genomic sequences. We found that these AMPs indeed suppress the growth of eight different strains of C. bombi , and that combinations of AMPs were typically more effective than the use of a single AMP alone. Furthermore, the most effective combinations were rarely those consisting of maximum concentrations. In addition, the AMP combination treatments revealed parasite strain specificity, such that strains varied in their sensitivity towards the same mixtures. Hence, variable expression of AMPs could be an alternative strategy to combat highly variable infections. This article is part of the themed issue ‘Evolutionary ecology of arthropod antimicrobial peptides’.

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Immune response and gut microbial community structure in bumblebees after microbiota transplants

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2016.0312 ◽

2016 ◽

Vol 283 (1831) ◽

pp. 20160312 ◽

Cited By ~ 17

Author(s):

Kathrin Näpflin ◽

Paul Schmid-Hempel

Keyword(s):

Immune Response ◽

Immune System ◽

Microbial Community ◽

Bombus Terrestris ◽

Microbial Community Composition ◽

Host Immune System ◽

Susceptible Host ◽

Protective Function ◽

Crithidia Bombi ◽

Gut Microbial Community

Microbial communities are a key component of host health. As the microbiota is initially ‘foreign’ to a host, the host's immune system should respond to its acquisition. Such variation in the response should relate not only to host genetic background, but also to differences in the beneficial properties of the microbiota. However, little is known about such interactions. Here, we investigate the gut microbiota of the bumblebee, Bombus terrestris , which has a protective function against the bee's natural trypanosome gut parasite, Crithidia bombi . We transplanted ‘resistant’ and ‘susceptible’ microbiota into ‘resistant’ and ‘susceptible’ host backgrounds, and studied the activity of the host immune system. We found that bees from different resistance backgrounds receiving a microbiota differed in aspects of their immune response. At the same time, the elicited immune response also depended on the received microbiota's resistance phenotype. Furthermore, the microbial community composition differed between microbiota resistance phenotypes (resistant versus susceptible). Our results underline the complex feedback between the host's ability to potentially exert selection on the establishment of a microbial community and the influence of the microbial community on the host immune response in turn.

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Protein-poor diet reduces host-specific immune gene expression in Bombus terrestris

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2014.0128 ◽

2014 ◽

Vol 281 (1786) ◽

pp. 20140128 ◽

Cited By ~ 65

Author(s):

Franziska S. Brunner ◽

Paul Schmid-Hempel ◽

Seth M. Barribeau

Keyword(s):

Immune Responses ◽

Bombus Terrestris ◽

Expression Patterns ◽

Resource Limitation ◽

Immune Gene ◽

Individual Level ◽

Nutritional Limitation ◽

Trade Offs ◽

Crithidia Bombi ◽

The Individual

Parasites infect hosts non-randomly as genotypes of hosts vary in susceptibility to the same genotypes of parasites, but this specificity may be modulated by environmental factors such as nutrition. Nutrition plays an important role for any physiological investment. As immune responses are costly, resource limitation should negatively affect immunity through trade-offs with other physiological requirements. Consequently, nutritional limitation should diminish immune capacity in general, but does it also dampen differences among hosts? We investigated the effect of short-term pollen deprivation on the immune responses of our model host Bombus terrestris when infected with the highly prevalent natural parasite Crithidia bombi . Bumblebees deprived of pollen, their protein source, show reduced immune responses to infection. They failed to upregulate a number of genes, including antimicrobial peptides, in response to infection. In particular, they also showed less specific immune expression patterns across individuals and colonies. These findings provide evidence for how immune responses on the individual-level vary with important elements of the environment and illustrate how nutrition can functionally alter not only general resistance, but also alter the pattern of specific host–parasite interactions.

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The impact of host starvation on parasite development and population dynamics in an intestinal trypanosome parasite of bumble bees

Parasitology ◽

10.1017/s0031182005007304 ◽

2005 ◽

Vol 130 (6) ◽

pp. 637-642 ◽

Cited By ~ 49

Author(s):

A. LOGAN ◽

M. X. RUIZ-GONZÁLEZ ◽

M. J. F. BROWN

Keyword(s):

Population Dynamics ◽

Developmental Process ◽

Bombus Terrestris ◽

Parasite Development ◽

Parasitic Infections ◽

Parasite Transmission ◽

Crithidia Bombi ◽

Host Nutrition ◽

Vertebrate Hosts ◽

The Impact

Host nutrition plays an important role in determining the development and success of parasitic infections. While studies of vertebrate hosts are accumulating, little is known about how host nutrition affects parasites of invertebrate hosts.Crithidia bombiis a gut trypanosome parasite of the bumble bee,Bombus terrestrisand here we use it as a model system to determine the impact of host nutrition on the population dynamics and development of micro-parasites in invertebrates. Pollen-starved bees supported significantly smaller populations of the parasite. In pollen-fed bees the parasite showed a temporal pattern in development, with promastigote transmission stages appearing at the start of the infection and gradually being replaced by choanomastigote and amastigote forms. In pollen-starved bees this developmental process was disrupted, and there was no pattern in the appearance of these three forms. We discuss the implications of these results for parasite transmission, and speculate about the mechanisms behind these changes.

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