Immune Gene Expression in Bombus terrestris: Signatures of Infection Despite Strong Variation among Populations, Colonies, and Sister Workers

Brunner, Franziska S.; Schmid‐Hempel, Paul; Barribeau, Seth M.

doi:10.1371/journal.pone.0068181

Cited by 43 publications

(55 citation statements)

References 42 publications

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“…Previous studies have shown that parasite challenge can induce various alterations of the immune system of bees (e.g. [52,53]), and this, even without actual successful infection and production of spores, can impair the learning and memory of bees as shown by stimulating the immune system of honeybees and bumblebees with non-pathogenic elicitors, lipopolysaccharides [14,15,51].…”

Section: Discussionmentioning

confidence: 99%

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Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honeybees and bumblebees

Piiroinen¹,

Goulson²

2016

Proc. R. Soc. B.

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Learning and memory are crucial functions which enable insect pollinators to efficiently locate and extract floral rewards. Exposure to pesticides or infection by parasites may cause subtle but ecologically important changes in cognitive functions of pollinators. The potential interactive effects of these stressors on learning and memory have not yet been explored. Furthermore, sensitivity to stressors may differ between species, but few studies have compared responses in different species. Here, we show that chronic exposure to fieldrealistic levels of the neonicotinoid clothianidin impaired olfactory learning acquisition in honeybees, leading to potential impacts on colony fitness, but not in bumblebees. Infection by the microsporidian parasite Nosema ceranae slightly impaired learning in honeybees, but no interactive effects were observed. Nosema did not infect bumblebees (3% infection success). Nevertheless, Nosema-treated bumblebees had a slightly lower rate of learning than controls, but faster learning in combination with neonicotinoid exposure. This highlights the potential for complex interactive effects of stressors on learning. Our results underline that one cannot readily extrapolate findings from one bee species to others. This has important implications for regulatory risk assessments which generally use honeybees as a model for all bees.

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Section: Discussionmentioning

confidence: 99%

“…An altered immune system as discussed above [15,53] could potentially explain the lower learning rate in Nosema-inoculated bumblebees, suggesting that ingestion of spores solely may be stressful for bumblebees. The low infectivity of bumblebees is intriguing given our preliminary tests showed that 60% of the inoculated bees became infected.…”

Section: Discussionmentioning

confidence: 99%

Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honeybees and bumblebees

Piiroinen¹,

Goulson²

2016

Proc. R. Soc. B.

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“…Six colonies were used for this experiment, three with ancestors from Aesch (colonies 2, 4 and 6) and three with ancestors from Neunforn (colonies 1, 5 and 9). Queens of these two collection sites differ in infection prevalence with our model parasite C. bombi [31].…”

Section: Materials and Methods (A) Bee Breeding And Treatmentmentioning

confidence: 99%

“…Generally, infection with C. bombi increases expression of genes encoding AMPs and immune pathway signalling genes shortly after infection [31,32,39], and the putative recognition molecule haemomucin after infection establishment [40]. Wounding and bacterial infection of B. terrestris workers also increases AMP expression and decreases expression of signalling and other effector genes [41].…”

Section: Introductionmentioning

confidence: 99%

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

2014

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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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“…Interestingly, the expression of defense genes shows elevated levels of additive genetic variance in Drosophila species, which can indicate balancing selection (27) and can result from frequency-dependent selection as in Red Queen host-parasite dynamics. Indeed, host gene expression responses vary with host genotype in several systems [e.g., Drosophila melanogaster (28), Apis mellifera (29), Bombus terrestris (30)(31)(32), and Mus musculus (32)]. Similarly, some studies have described variation in host expression depending on parasite genotype (33)(34)(35).…”

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confidence: 99%

Gene expression differences underlying genotype-by-genotype specificity in a host–parasite system

Barribeau

Sadd

Plessis

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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113

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In many systems, host-parasite evolutionary dynamics have led to the emergence and maintenance of diverse parasite and host genotypes within the same population. Genotypes vary in key attributes: Parasite genotypes vary in ability to infect, host genotypes vary in susceptibility, and infection outcome is frequently the result of both parties' genotypic identities. These host-parasite genotype-by-genotype (G H × G P ) interactions influence evolutionary and ecological dynamics in important ways. Interactions can be produced through genetic variation; however, here, we assess the role of variable gene expression as an additional source of G H × G P interactions. The bumblebee Bombus terrestris and its trypanosome gut parasite Crithidia bombi are a model system for host-parasite matching. Full-transcriptome sequencing of the bumblebee host revealed that different parasite genotypes indeed induce fundamentally different host expression responses and host genotypes vary in their responses to the infecting parasite genotype. It appears that broadly and successfully infecting parasite genotypes lead to reduced host immune gene expression relative to unexposed bees but induce the expression of genes responsible for controlling gene expression. Contrastingly, a poorly infecting parasite genotype induced the expression of immunologically important genes, including antimicrobial peptides. A targeted expression assay confirmed the transcriptome results and also revealed strong host genotype effects. In all, the expression of a number of genes depends on the host genotype and the parasite genotype and the interaction between both host and parasite genotypes. These results suggest that alongside sequence variation in coding immunological genes, variation that controls immune gene expression can also produce patterns of host-parasite specificity.coevolution | manipulation | Red Queen

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Immune Gene Expression in Bombus terrestris: Signatures of Infection Despite Strong Variation among Populations, Colonies, and Sister Workers

Cited by 43 publications

References 42 publications

Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honeybees and bumblebees

Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honeybees and bumblebees

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

Gene expression differences underlying genotype-by-genotype specificity in a host–parasite system

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