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

MicrobiologyOpen

Volumn 1, Issue 4, 2012, Pages 362-372

  Popp, Mario ^a   Erler, Silvio ^a   Lattorff, H Michael G ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

Effective population size; Heterozygosity; Host parasite interaction; Intensity of infection; Multiple infections

Indexed keywords

ANIMAL TISSUE; ARTICLE; BUMBLEBEE; CONTROLLED STUDY; CRITHIDIA; CRITHIDIA BOMBI; EFFECTIVE POPULATION SIZE; FORAGING; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENETIC SELECTION; GENETIC VARIABILITY; HOMOZYGOSITY; HOST PARASITE INTERACTION; INFECTION RATE; INTERSPECIFIC RELATIONSHIP; MIXED INFECTION; NONHUMAN; PARASITE TRANSMISSION; PREVALENCE; PRIORITY JOURNAL; SEASONAL VARIATION; TRYPANOSOMIASIS;

EID: 84892540489     PISSN: None     EISSN: 20458827     Source Type: Journal    
DOI: 10.1002/mbo3.35     Document Type: Article

References (42)

1. Akopyants, N. S., N. Kimblin, N. Secundino, R. Patrick, N. Peters, P. Lawyer, et al. 2009. Demonstration of genetic exchange during cyclical development of Leishmania in the sand fly vector. Science 324:265-268.
2. Alford, D. V. 1975. Bumblebees. Davis-Poynter, London, U.K.
3. Alford, D. V. 1978. The life of the bumblebee. Davis-Poynter, London, U.K.
4. Araki, H., R. S. Waples, and M. S. Blouin. 2007. A potential bias in the temporal method for estimating Ne in admixed populations under natural selection. Mol. Ecol. 16:2261-2271.
5. Boomsma, J. J., and F. L. W. Ratnieks. 1996. Paternity in eusocial Hymenoptera. Philos. Trans. R. Soc. Lond. B Biol. Sci. 351:947-975.
6. Brown, M. J. F., R. Schmid-Hempel, and P. Schmid-Hempel. 2003. Strong context-dependent virulence in a host-parasite system: reconciling genetic evidence with theory. J. Anim. Ecol. 72:994-1002.
7. Clark, T. B. 1977. Spiroplasma sp. as a new pathogen in the honeybees. J. Invertebr. Pathol. 29:112-113.
8. Cornuet, J. M., and F. Aries. 1980. Number of sex alleles in a sample of honeybee colonies. Apidologie 11:87-93.
9. Day, K. P., J. C. Koella, S. Nee, S. Gupta, and A. F. Read. 1992. Population genetics and dynamics of Plasmodium falciparum - an ecological view. Parasitology (Suppl.) 104:S35-S52.
10. Durrer, S., and P. Schmid-Hempel. 1994. Shared use of flowers leads to horizontal pathogen transmission. Proc. R. Soc. Lond. B Biol. Sci. 258:299-302.
11. Erler, S., and H. M. G. Lattorff. 2010. The degree of parasitism of the bumblebee (Bombus terrestris) by cuckoo bumblebees (Bombus (Psithyrus) vestalis). Insectes Soc. 57:371-377.
12. Erler, S., M. Popp, S. Wolf, H. Lattorff, and G. Michael. 2012. Sex, horizontal transmission, and multiple hosts prevent local adaptation of Crithidia bombi, a parasite of bumblebees (Bombus spp.). Ecol. Evol. 2:930-940.
13. Estoup, A., A. Scholl, A. Pouvreau, and M. Solignac. 1995. Monoandry and polyandry in bumble bees (Hymenoptera; Bombinae) as evidenced by highly variable microsatellites. Mol. Ecol. 4:89-93.
14. Estoup, A., M. Solignac, J. M. Cornuet, J. Goudet, and A. Scholl. 1996. Genetic differentiation of continental and island populations of Bombus terrestris (Hymenoptera: Apidae) in Europe. Mol. Ecol. 5:19-31.
15. Fouks, B., and H. M. G. Lattorff. 2011. Recognition and avoidance of contaminated flowers by foraging bumblebees (Bombus terrestris). PLoS ONE 6:e26328.
16. Frank, S. A. 1992. A kin selection model for the evolution of virulence. Proc. R. Soc. Lond. B Biol. Sci. 250:195-197.
17. Gillespie, S. 2010. Factors affecting parasite prevalence among wild bumblebees. Ecol. Entomol. 35:737-747.
18. Goulson, D., O. Lepais, S. O'Connor, J. L. Osborne, R. A. Sanderson, J. Cussans, et al. 2010. Effects of land use at a landscape scale on bumblebee nest density and survival. J. Appl. Ecol. 47:1207-1215.
19. Levin, S. A., and D. Pimentel. 2001. Host life history and the evolution of parasite virulence. Evolution 55:1056-1062.
20. Lipa, J. J., and O. Triggiani. 1988. Crithidia bombi sp. n. a flagellated parasite of a bumble-bee Bombus terrestris L. (Hymenoptera, Apidae). Acta Protozool. 27:287-290.
21. Manson, J. S., M. C. Otterstatter, and J. D. Thomson. 2010. Consumption of a nectar alkaloid reduces pathogen load in bumble bees. Oecologia 162:81-89.
22. Mauss, V. 1994. Bestimmungsschlüssel für Hummeln. Deutscher Jugendbund für Naturbeobachtungen (DJN), Hamburg, Germany.
23. Moritz, R. F. A., H. Scharpenberg, H. M. G. Lattorff, and P. Neumann. 2003. A technical note for using microsatellite DNA analyses in haploid male DNA pools of social Hymenoptera. Insectes Soc. 50:398-400.
24. Popp, M., and H. M. G. Lattorff. 2011. A quantitative in vitro cultivation technique to determine cell number and growth rates in strains of Crithidia bombi (Trypanosomatidae), a parasite of bumblebees. J. Eukaryot. Microbiol. 58:7-10.
25. Read, A. F., and L. H. Taylor. 2001. The ecology of genetically diverse infections. Science 292:1099-1102.
26. Riddell, C. E., S. Adams, P. Schmid-Hempel, and E. B. Mallon. 2009. Differential expression of immune defences is associated with specific host-parasite interactions in insects. PLoS ONE 4:e7621.
27. Riddell, C. E., S. Sumner, S. Adams, and E. B. Mallon. 2011. Pathways to immunity: temporal dynamics of the bumblebee (Bombus terrestris) immune response against a trypanosomal gut parasite. Insect Mol. Biol. 20:529-540.
28. Ruiz-Gonzáles, M. X., J. Bryden, Y. Moret, C. Reber-Funk, P. Schmid-Hempel, and M. J. F. Brown. 2012. Dynamic transmission, host quality, and population structure in a multi host parasite of bumblebees. Evolution. doi: 10.1111/j.1558-5646.2012.01655.x.
29. Salathé, R. M., and P. Schmid-Hempel. 2011. The genotypic structure of a multi-host bumblebee parasite suggests a role for ecological niche overlap. PLoS ONE 6:e22054.
30. Schjorring, S., and J. C. Koella. 2003. Sub-lethal effects of pathogens can lead to the evolution of lower virulence in multiple infections. Proc. R. Soc. Lond. B Biol. Sci. 270:189-193.
31. Schlüns, H., B. M. Sadd, P. Schmid-Hempel, and R. H. Crozier. 2010. Infection with the trypanosome Crithidia bombi and expression of immune-related genes in the bumblebee Bombus terrestris. Dev. Comp. Immunol. 34:705-709.
32. Schmid-Hempel, P. 1998. Parasites in social insects. Princeton University Press, Princeton, NJ.
33. Schmid-Hempel, P., and C. Reber-Funk. 2004. The distribution of genotypes of the trypanosome parasite, Crithidia bombi, in populations of its host, Bombus terrestris. Parasitology 129:147-158.
34. Schmid-Hempel, R., and P. Schmid-Hempel. 2000. Female mating frequencies in Bombus spp. from Central Europe. Insectes Soc. 47:36-41.
35. Schmid-Hempel, P., K. Puhr, N. Krüger, C. Reber, and R. Schmid-Hempel. 1999. Dynamic and genetic consequences of variation in horizontal transmission for a microparasitic infection. Evolution 53:426-434.
36. Schmid-Hempel, R., R. Salathé, M. Tognazzo, and P. Schmid-Hempel. 2011. Genetic exchange of novel strains in directly transmitted trypanosomatids. Infect. Genet. Evol. 11:564-571.
37. Shykoff, J. A., and P. Schmid-Hempel. 1991. Incidence and effects of four parasites in populations of bumble bees in Switzerland. Apidologie 22:117-225.
38. Shykoff, J. A., and P. Schmid-Hempel. 1992. Parasites delay worker reproduction in the bumblebee: consequences for eusociality. Behav. Ecol. 2:242-248.
39. Ulrich, Y., B. M. Sadd, and P. Schmid-Hempel. 2011. Strain filtering and transmission of a mixed infection in a social insect. J. Evol. Biol. 24:354-362.
40. Walsh, P. S., D. A. Metzger, and R. Higuchi. 1991. Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506-513.
41. Wang, J. L. 2004. Sibship reconstruction from genetic data with typing errors. Genetics 166:1963-1979.
42. Whitehorn, P. R., M. C. Tinsley, M. J. F. Brown, B. Darvill, and D. Goulson. 2011. Genetic diversity, parasite prevalence and immunity in wild bumblebees. Proc. R. Soc. Lond. B Biol. Sci. 278:1195-1202.