Dataset Information

Seasonal variability of prevalence and occurrence of multiple infections shape the population structure of Crithidia bombi, an intestinal parasite of bumblebees (Bombus spp.).

ABSTRACT: Ergonomic growth phases of annual social insect societies strongly influence horizontally transmitted parasites. Herein, we focused on the impact of temporal changes in host demography on the population structure of a horizontally transmitted parasite. Seasonal fluctuations in prevalence and the occurrence of multiple infections of the gut parasite Crithidia bombi were analyzed in repeatedly sampled populations of two common bumblebee (Bombus spp.) species. Prevalence of C. bombi was greatest in the middle of the foraging season and coincided with the maximal occurrence of multiple infections. Both decline later in the season. The genetic structure of the parasite population also showed strong seasonal fluctuations with a drastic decline in effective population size and an increase in linkage disequilibrium when infection rates were highest. These effects are mainly attributable to significant changes in parasite allele frequencies leading to selection of specific alleles and increasing the frequency of homozygote genotypes in the middle of the season. Within host, competition between parasite genotypes might explain the observed pattern leading to selection of these alleles, and thus a boost of homozygote genotypes in the middle of the season. Toward the end of the season, selection appears to relax and we observed a recovery in linkage equilibrium, as well as an increase in effective population size. This might be explained by genetic exchange in these trypanosomes in natural populations.

SUBMITTER: Popp M

PROVIDER: S-EPMC3535382 | biostudies-literature | 2012 Dec

REPOSITORIES: biostudies-literature

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Seasonal variability of prevalence and occurrence of multiple infections shape the population structure of Crithidia bombi, an intestinal parasite of bumblebees (Bombus spp.).

Popp Mario M Erler Silvio S Lattorff H Michael G HM

MicrobiologyOpen 20120923 4

Ergonomic growth phases of annual social insect societies strongly influence horizontally transmitted parasites. Herein, we focused on the impact of temporal changes in host demography on the population structure of a horizontally transmitted parasite. Seasonal fluctuations in prevalence and the occurrence of multiple infections of the gut parasite Crithidia bombi were analyzed in repeatedly sampled populations of two common bumblebee (Bombus spp.) species. Prevalence of C. bombi was greatest in ...[more]

PMID: 23233373

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Project description:Trypanosomatids (Trypanosomatidae, Kinetoplastida) are flagellated protozoa containing many parasites of medical or agricultural importance. Among those, Crithidia bombi and C. expoeki, are common parasites in bumble bees around the world, and phylogenetically close to Leishmania and Leptomonas. They have a simple and direct life cycle with one host, and partially castrate the founding queens greatly reducing their fitness. Here, we report the nuclear genome sequences of one clone of each species, extracted from a field-collected infection. Using a combination of Roche 454 FLX Titanium, Pacific Biosciences PacBio RS, and Illumina GA2 instruments for C. bombi, and PacBio for C. expoeki, we could produce high-quality and well resolved sequences. We find that these genomes are around 32 and 34 MB, with 7,808 and 7,851 annotated genes for C. bombi and C. expoeki, respectively-which is somewhat less than reported from other trypanosomatids, with few introns, and organized in polycistronic units. A large fraction of genes received plausible functional support in comparison primarily with Leishmania and Trypanosoma. Comparing the annotated genes of the two species with those of six other trypanosomatids (C. fasciculata, L. pyrrhocoris, L. seymouri, B. ayalai, L. major, and T. brucei) shows similar gene repertoires and many orthologs. Similar to other trypanosomatids, we also find signs of concerted evolution in genes putatively involved in the interaction with the host, a high degree of synteny between C. bombi and C. expoeki, and considerable overlap with several other species in the set. A total of 86 orthologous gene groups show signatures of positive selection in the branch leading to the two Crithidia under study, mostly of unknown function. As an example, we examined the initiating glycosylation pathway of surface components in C. bombi, finding it deviates from most other eukaryotes and also from other kinetoplastids, which may indicate rapid evolution in the extracellular matrix that is involved in interactions with the host. Bumble bees are important pollinators and Crithidia-infections are suspected to cause substantial selection pressure on their host populations. These newly sequenced genomes provide tools that should help better understand host-parasite interactions in these pollinator pathogens.

Project description:Recent declines in bumble bee populations are of great concern and have prompted critical evaluations of the role of pathogen introductions and host resistance in bee health. One factor that may influence host resilience when facing infection is the gut microbiota. Previous experiments with Bombus terrestris, a European bumble bee, showed that the gut microbiota can protect against Crithidia bombi, a widespread trypanosomatid parasite of bumble bees. However, the particular characteristics of the microbiome responsible for this protective effect have thus far eluded identification. Using wild and commercially sourced Bombus impatiens, an important North American pollinator, we conducted cross-wise microbiota transplants to naive hosts of both backgrounds and challenged them with a Crithidia parasite. As with B. terrestris, we find that microbiota-dependent protection against Crithidia operates in B. impatiens Lower Crithidia infection loads were experimentally associated with high microbiome diversity, large gut bacterial populations, and the presence of Apibacter, Lactobacillus Firm-5, and Gilliamella spp. in the gut community. These results indicate that even subtle differences between gut community structures can have a significant impact on a microbiome's ability to defend against parasite infections.IMPORTANCE Many wild bumble bee populations are under threat due to human activity, including through the introduction of pathogens via commercially raised bees. Recently, it was found that the bumble bee gut microbiota can help defend against a common parasite, Crithidia bombi, but the particular factors contributing to this protection are unknown. Using both wild and commercially raised bees, we conducted microbiota transplants to show that microbiome diversity, total gut bacterial load, and the presence of certain core members of the microbiota may all impact bee susceptibility to Crithidia infection. Bee origin (genetic background) was also a factor. Finally, by examining this phenomenon in a previously uninvestigated bee species, our study demonstrates that microbiome-mediated resistance to Crithidia is conserved across multiple bumble bee species. These findings highlight how intricate interactions between hosts, microbiomes, and parasites can have wide-ranging consequences for the health of ecologically important species.

Project description:BackgroundAccurate estimates of movement behavior and distances travelled by animals are difficult to obtain, especially for small-bodied insects where transmitter weights have prevented the use of radio-tracking.Methodology/principal findingsHere, we report the first successful use of micro radio telemetry to track flight distances and space use of bumblebees. Using ground surveys and Cessna overflights in a Central European rural landscape mosaic we obtained maximum flight distances of 2.5 km, 1.9 km and 1.3 km for Bombus terrestris (workers), Bombus ruderatus (worker), and Bombus hortorum (young queens), respectively. Bumblebee individuals used large areas (0.25-43.53 ha) within one or a few days. Habitat analyses of one B. hortorum queen at the landscape scale indicated that gardens within villages were used more often than expected from habitat availability. Detailed movement trajectories of this individual revealed that prominent landscape structures (e.g. trees) and flower patches were repeatedly visited. However, we also observed long (i.e. >45 min) resting periods between flights (B. hortorum) and differences in flower-handling between bumblebees with and without transmitters (B. terrestris) suggesting that the current weight of transmitters (200 mg) may still impose significant energetic costs on the insects.Conclusions/significanceSpatio-temporal movements of bumblebees can now be tracked with telemetry methods. Our measured flight distances exceed many previous estimates of bumblebee foraging ranges and suggest that travelling long distances to food resources may be common. However, even the smallest currently available transmitters still appear to compromise flower handling performance and cause an increase in resting behavior of bees. Future reductions of transmitter mass and size could open up new avenues for quantifying landscape-scale space use of insect pollinators and could provide novel insights into the behavior and requirements of bumblebees during critical life stages, e.g. when searching for mates, nest locations or hibernation sites.

Dataset Information

Seasonal variability of prevalence and occurrence of multiple infections shape the population structure of Crithidia bombi, an intestinal parasite of bumblebees (Bombus spp.).

Publications

Seasonal variability of prevalence and occurrence of multiple infections shape the population structure of Crithidia bombi, an intestinal parasite of bumblebees (Bombus spp.).

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