Sex, horizontal transmission, and multiple hosts prevent local adaptation of Crithidia bombi, a parasite of bumblebees (Bombus spp.)

Ecology and Evolution

Volumn 2, Issue 5, 2012, Pages 930-940

  Erler, Silvio ^a,b   Popp, Mario ^a   Wolf, Stephan ^a,c   Lattorff, H Michael G ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b Univ de tiin e Agricole i Medicin Veterinar   (Romania)

^c ROTHAMSTED RESEARCH   (United Kingdom)

Author keywords

Bombus; Bumblebee; Coevolution; Crithidia bombi; Host parasite interaction; Population genetic structure

Indexed keywords

EID: 84871769353     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.250     Document Type: Article

References (52)

1. Akopyants,N. S., N. Kimblin, N. Secundino, R. Patrick, N. Peters, P. Lawyer, D. E. Dobson, S. M. Beverley, and D. L. Sacks. 2009. Demonstration of genetic exchange during cyclical development of Leishmania in the sand fly vector. Science 324:265-268.
2. 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.
3. Cameron, S. A., H. M. Hines, and P. H.Williams. 2007. A comprehensive phylogeny of the bumble bees (Bombus). Biol. J. Linn. Soc. 91:161-188.
4. Cornuet, J.-M., and F. Aries. 1980. Number of sex alleles in a sample of honeybee colonies. Apidologie 11:87-93.
5. Durrer, S., and P. Schmid-Hempel. 1994. Shared use of flowers leads to horizontal pathogen transmission. Proc. R. Soc. Lond. B 258:299-302.
6. Erler, S., and H. M. G. Lattorff. 2010. The degree of parasitism of the bumblebee (Bombus terrestris) by cuckoo bumblebees (Bombus (Psithyrus) vestalis). Insectes Sociaux 57:371- 377.
7. Erler, S., M. Popp, and H. M. G. Lattorff. 2011. Dynamics of immune system gene expression upon bacterial challenge and wounding in a social insect (Bombus terrestris). PLoS One 6:e18126.
8. 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.
9. 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.
10. Excoffier, L., G. Laval, and S. Schneider. 2005. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol. Bioinform. Online 1:47-50.
11. Lajeunesse, M. J., and M. R. Forbes. 2002. Host range and local parasite adaptation. Proc. R. Soc. Lond. B 269:703-710.
12. Fouks, B., and H. M. G. Lattorff. 2011. Recognition and avoidance of contaminated flowers by foraging bumblebees (Bombus terrestris). PLoS One 6:e26328.
13. Gillespie, S. 2010. Factors affecting parasite prevalence among wild bumblebees. Ecol. Entomol. 35:737-747.
14. Goulson, D. 2010. Bumblebees behaviour, ecology, and conservation. Oxford Univ. Press, Oxford, NY.
15. Goulson, D., and B. Darvill. 2004. Niche overlap and diet breadth in bumblebees; are rare species more specialized in their choice of flowers? Apidologie 53:55-63.
16. Goulson, D., and J. L. Osborne. 2009. Foraging range and the spatial distribution of worker bumble bees. Pp. 97-111 in S. Jarau and M. Hrncir, eds. Food exploitation by social insects, ecological, behavioral, and theoretical approaches. CRC Press, Boca Raton, FL.
17. Goulson, D., O. Lepais, S. O'Connor, J. L. Osborne, R. A. Sanderson, J. Cussans, L. Goffe, and B. Darvill. 2010. Effects of land use at a landscape scale on bumblebee nest density and survival. J. Appl. Ecol. 47:1207-1215.
18. Imhoof, B., and P. Schmid-Hempel. 1998. Patterns of local adaptation of a protozoan parasite to its bumblebee host. Oikos 82:59-66.
19. Imhoof, B., and P. Schmid-Hempel. 1999. Colony success of the bumble bee, Bombus terrestris, in relation to infections by two protozoan parasites, Crithidia bombi and Nosema bombi. Insectes Sociaux 46:233-238.
20. Kalinowski, S. T. 2005. HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol. Ecol. Notes 5:187-189.
21. Kraus, F. B., S.Wolf, and R. F. A. Moritz. 2009. Male flight distance and population substructure in the bumblebee Bombus terrestris. J. Anim. Ecol. 78:247-252.
22. Lepais, O., B. Darvill, S. O'Connor, J. L. Osborne, R. A. Sanderson, J. Cussans, L. Goffe, and D. Goulson. 2010. Estimation of bumblebee queen dispersal distances using sibship reconstruction method. Mol. Ecol. 19:819-831.
23. 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.
24. Loken, A. 1984. Scandinavian species of the genus Psithyrus Lepeletier (Hymenoptera: Apidae). Entomol. Scand. Suppl. 23:1-45.
25. Mauss, V. 1994. Bestimmungsschlüssel für Hummeln. Deutscher Jugendbund für Naturbeobachtungen (DJN), Hamburg.
26. McGhee, R. B., andW. Cosgrove. 1980. Biology and physiology of the lower Trypanosomatidae. Microbiol. Rev. 44:140-173.
27. Pritchard, J. K., M. Stephens, and P. Donnelly. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
28. Popp, M., S. Erler, and H. M. G. Lattorff. 2012. Seasonal variability of prevalence and occurrence of multiple infections shapes the population structure of Crithidia bombi, an intestinal parasite of bumblebees (Bombus spp.). Environ. Microbiol. (under review)
29. Raymond, M., and F. Rousset. 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86:248-249.
30. 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.
31. 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.
32. Rousset, F. 2008. Genepop'007: a complete reimplementation of the Genepop software forWindows and Linux. Mol. Ecol. Res. 8:103-106.
33. 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.
34. Schmid-Hempel, P. 1995. Parasites and social insects. Apidologie 26:255-271.
35. Schmid-Hempel, P. 1998. Parasites in social insects. Princeton Univ. Press, Princeton, NJ.
36. 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.
37. Schmid-Hempel, R., and P. Schmid-Hempel. 2000. Female mating frequencies in Bombus spp. from Central Europe. Insectes Sociaux 47:36-41.
38. Schmid-Hempel, R., R. Salathé, M. Tognazzo, and P. Schmid-Hempel. 2011. Genetic exchange and emergence of novel strains in directly transmitted trypanosomatids. Infect. Genet. Evol. 11:564-571.
39. Schurko, A. M., M. Neiman, and J. M. Logsdon. 2009. Signs of sex: what we know and how we know it. Trends Ecol. Evol. 24:208-217.
40. Shykoff, J. A., and P. Schmid-Hempel. 1991a Parasites delay worker reproduction in bumblebees: consequences for eusociality. Behav. Ecol. 2:242-248.
41. Shykoff, J. A., and P. Schmid-Hempel. 1991b Incidence and effects of four parasites in natural populations of bumble bees in Switzerland. Apidologie 22:117-125.
42. Sladen, F.W. L. 1912. The humble-bee-its life-history and how to domesticate it. Macmillan and co., limited, London.
43. Stenberg, P., M. Lundmark, and A. Saura. 2003. MLGsim: a program for detecting clones using a simulation approach. Mol. Ecol. Notes 3:329-331.
44. 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.
45. von Hagen, E., and A. Aichhorn. 2003. Hummel: bestimmen, ansiedeln, vermehren, schützen. Fauna-Verlag, Nottuln, Germany.
46. 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.
47. Wang, J. L. 2004. Sibship reconstruction from genetic data with typing errors. Genetics 166:1963-1979.
48. Whitehorn, P. R.,M. C. Tinsley, M. J. F. Brown, B. Darvill, andD. Goulson. 2010. Genetic diversity, parasite prevalence and immunity in wild bumblebees. Proc. R. Soc. B 278:1195-1202.
49. Wolf, S., and R. F. A. Moritz. 2008. Foraging distance in Bombus terrestris L. (Hymenoptera: Apidae). Apidologie 39:419-427.
50. Wolf, S., T. Toev, R. L. V.Moritz, and R. F. A.Moritz. 2012. Spatial and temporal dynamics of the male effective population size in bumblebees (Hymenoptera: Apidae). Popul. Ecol. 54:115-124.
51. Yourth, C. P., and P. Schmid-Hempel. 2006. Serial passage of the parasite Crithidia bombi within a colony of its host, Bombus terrestris, reduces success in unrelated hosts. Proc. R. Soc. B 273:655-659.
52. Yourth, C. P., M. J. F. Brown, and P. Schmid-Hempel. 2008. Effects of natal and novel Crithidia bombi (Trypanosomatidae) infections on Bombus terrestris hosts. Insectes Sociaux 55:86-90.