Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-27T20:58:29.707Z Has data issue: false hasContentIssue false

Chapter one - Pollinator diseases: the Bombus–Crithidia system

from Part I - Understanding within-host processes

Published online by Cambridge University Press:  28 October 2019

By
Paul Schmid-Hempel ,
Lena Wilfert  and
Regula Schmid-Hempel
Edited by
Kenneth Wilson ,
Andy Fenton  and
Dan Tompkins
Kenneth Wilson
Affiliation:
Lancaster University
Andy Fenton
Affiliation:
University of Liverpool
Dan Tompkins
Affiliation:
Predator Free 2050 Ltd
Get access

Summary

Several species of Crithidia are gut parasites of bumble bees (Bombus spp.), their main effect being to castrate the queens emerging from hibernation. The parasites are common in natural populations, spread among colonies and host species by shared use of flowers. Infection prevalence varies on a small geographic scale and over years, with no clear pattern. Genetic analyses of C. bombi show that mixed-genotype infections of single host individuals are common, associated with a high rate of sexual reproduction inside the host. Parasite populations are genotypically highly diverse, with up to 30 concurrent infections, such that the same genotype is rarely found more than once in a sample. A hallmark of this system is that a given parasite genotype infects only a certain range of host genotypic backgrounds, and this range varies among parasite genotypes. Hosts are susceptible to a limited range of parasite genotypes. A major defence Bombus uses against Crithidia is deployment of anti-microbial peptides (AMPs), which have been characterised with release of the Bombus genome. AMPs have synergistic effects. Queen mothers can also protect their offspring, the workers in the colony, by trans-generational immune priming.

Keywords

Parasite diversitylong-term prevalencebumblebeetrypanosomeCrithidiagenotypesgeographic variation.
Type
Chapter
Information
Wildlife Disease Ecology
Linking Theory to Data and Application
 , pp. 3 - 31
Publisher: Cambridge University Press
Print publication year: 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abbott, K.R. (2006) Bumblebees avoid flowers containing evidence of past predation events. Canadian Journal of Zoology, 84, 1240–1247.Google Scholar
Akopyants, N.S., Kimbllin, N., Secundino, N., et al. (2009) Demonstration of genetic exchange during cyclical development of Leishmania in the sand fly vector. Science, 324, 265–268.Google Scholar
Anderson, R.M. & May, R.M. (1978) Regulation and stability of host–parasite population interactions. I. Regulatory processes. Journal of Animal Ecology, 47, 219–247.Google Scholar
Anderson, R.M. & May, R.M. (1982) Coevolution of hosts and parasites. Parasitology, 85, 411–426.Google Scholar
Antúnez, K., Martín-Hernández, R., Prieto, L., et al. (2009) Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environmental Microbiology, 11, 2284–2290.CrossRefGoogle ScholarPubMed
Baer, B. & Schmid-Hempel, P. (1999) Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature, 397, 151–154.Google Scholar
Baer, B. & Schmid-Hempel, P. (2003) Bumblebee workers from different sire groups vary in susceptibility to parasite infection. Ecology Letters, 6, 106–110.Google Scholar
Barribeau, S.M., Sadd, B., du Plessis, L., et al. (2015) A depauperate immune repertoire precedes evolution of sociality in bees. Genome Biology, 16, 83.Google Scholar
Barribeau, S.M., Sadd, B.M., du Plessis, L. & Schmid-Hempel, P. (2014) Gene expression differences underlying genotype-by-genotype specificity in a host–parasite system. Proceedings of the National Academy of Sciences of the United States of America, 111, 3496–3501.Google Scholar
Barribeau, S.M. & Schmid-Hempel, P. (2013) Qualitatively different immune response of the bumblebee host, Bombus terrestris, to infection by different genotypes of the trypanosome gut parasite, Crithidia bombi. Infection, Genetics and Evolution, 20, 249–256.Google Scholar
Barribeau, S.M., Schmid-Hempel, P. & Sadd, B. M. (2016) Royal decree: gene expression in transgenerationally immune primed bumblebee workers mimics a primary immune response. PLoS ONE, 11, e0159635.Google Scholar
Barry, J.D. & McCulloch, R. (2001) Antigenic variation in trypanosomes: enhanced phenotypic variation in a eukaryotic parasite. Advances in Parasitology, 49, 1–70.Google Scholar
Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., et al. (2006) Parallel declines on pollinators and insect-pollinated plants in Britain and the Netherlands. Science, 313, 351–354.Google Scholar
Blanford, S., Thomas, M.B., Pugh, C. & Pell, J.K. (2003) Temperature checks the Red Queen? Resistance and virulence in a fluctuating environment. Ecology Letters, 6, 2–5.Google Scholar
Brown, M.J.F., Loosli, R. & Schmid-Hempel, P. (2000) Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos, 91, 421–427.Google Scholar
Brown, M.J.F., Moret, Y. & Schmid-Hempel, P. (2003a) Activation of host constitutive immune defence by an intestinal trypanosome parasite of bumble bees. Parasitology, 126, 253–260.Google Scholar
Brown, M.J.F., Schmid-Hempel, R. & Schmid-Hempel, P. (2003b) Strong context-dependent virulence in a host–parasite system: reconciling genetic evidence with theory. Journal of Animal Ecology, 72, 994–1002.Google Scholar
Brunner, F.S., Schmid-Hempel, P. & Barribeau, S.M. (2013) Immune gene expression in Bombus terrestris: signatures of infection despite strong variation among populations, colonies, and sister workers. PLoS ONE, 8, e68181.Google Scholar
Cameron, S.A., Lozier, J.D., Strange, J.P., et al. (2011) Patterns of widespread decline in North American bumble bees. Proceedings of the National Academy of Sciences of the United States of America, 108, 662–667.Google Scholar
Carius, H.J., Little, T.J. & Ebert, D. (2001) Genetic variation in a host–parasite association: potential for coevolution and frequency-dependent selection. Evolution, 55, 1136–1145.Google Scholar
Cariveau, D.P., Powell, J.E., Koch, H., Winfree, R. & Moran, N.A. (2014) Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus). The ISME Journal, 8, 2369–2379.Google Scholar
Cisarovsky, G. & Schmid-Hempel, P. (2014a) Combining laboratory and field approaches to investigate the importance of flower nectar in the horizontal transmission of a bumblebee parasite. Entomologia Experimentalis et Applicata, 1–7, 1–7.Google Scholar
Cisarovsky, G. & Schmid-Hempel, P. (2014b) Few colonies of the host Bombus terrestris disproportionately affect the genetic diversity of its parasite, Crithidia bombi. Infection, Genetics and Evolution, 21, 192–197.Google Scholar
Cotter, S.C., Kruuk, L.E.B. & Wilson, K. (2004) Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. Journal of Evolutionary Biology, 17, 421–429.CrossRefGoogle Scholar
Cremer, S., Armitage, S.A.O. & Schmid-Hempel, P. (2007) Social immunity. Current Biology, 17, R693–R702.Google Scholar
Dawkins, R. (1982) The Extended Phenotype. Oxford: W.H. Freeman.Google Scholar
de Meeus, T., McCoy, K.D., Prugnolle, F., et al. (2006) Population genetics and molecular ecology or how to “debusquer la bête”. Infection, Genetics and Evolution, 7, 308–332.Google Scholar
Deshwal, S. & Mallon, E.B. (2014) Antimicrobial peptides play a functional role in bumblebee anti-trypanosome defense. Developmental & Comparative Immunology, 42, 240–243.Google Scholar
Dias, F.d.A., Vasconcellos, L.R.d.C., Romeiro, A., et al. (2014) Transovum transmission of trypanosomatid cysts in the milkweed bug, Oncopeltus fasciatus.PLoS ONE, 9, e108746.Google Scholar
Durrer, S. (1996) Parasite load and assemblages of bumblebee species. PhD thesis. Department of Environmental Sciences, ETH Zurich, Zürich: Verlag Studentenschaft.Google Scholar
Durrer, S. & Schmid-Hempel, P. (1994) Shared use of flowers leads to horizontal pathogen transmission. Proceedings of the Royal Society of London B, 258, 299–302.Google Scholar
Durrer, S. & Schmid-Hempel, P. (1995) Parasites and the regional distribution of bumble bee species. Ecography, 18, 114–122.Google Scholar
Dussaubat, C., Brunet, J.-L., Higes, M., et al. (2012) Gut pathology and responses to the microsporidium Nosema ceranae in the honey bee, Apis mellifera. PLoS ONE, 7, e37017.Google Scholar
Ebert, D., Duneau, D., Hall, M.D., et al. (2016) A population biology perspective on the stepwise infection process of the bacterial pathogen Pasteuria ramosa in Daphnia. Advances in Parasitology, 91, 265–310.Google Scholar
Engel, P., Martinson, V.G. & Moran, N.A. (2012) Functional diversity within the simple gut microbiota of the honey bee. Proceedings of the National Academy of Sciences of the United States of America, 109, 11,002–11,007.Google Scholar
Engel, P. & Moran, N.A. (2013a) Functional and evolutionary insights into the simple yet specific gut microbiota of the honey bee from metagenomic analysis. Gut Microbes, 4, 60–65.Google Scholar
Engel, P. & Moran, N.A. (2013b) The gut microbiota of insects – diversity in structure and function. FEMS Microbiological Reviews, 37, 699–735.Google Scholar
Erler, S., Popp, M., Wolf, S. & Lattorff, H.M.G. (2012) Sex, horizontal transmission, and multiple hosts prevent local adaptation of Crithidia bombi, a parasite of bumblebees (Bombus spp.). Ecology and Evolution, 2, 930–940.Google Scholar
Estoup, A., Solignac, M., Cornuet, J.M., Goudet, J. & Scholl, A. (1996) Genetic differentiation of continental and island populations of Bombus terrestris (Hymenoptera: Apidae) in Europe. Molecular Ecology, 5, 19–31.Google Scholar
Ewald, P.W. (1980) Evolutionary biology and the treatment of signs and symptoms of infectious disease. Journal of Theoretical Biology, 86, 169–176.Google Scholar
Ewald, P.W. (1983) Host–parasite relations, vectors, and the evolution of disease severity. Annual Review of Ecology and Systematics, 14, 465–485.Google Scholar
Fenton, A., Antonovics, J. & Brockhurst, M.A. (2009) Inverse gene-for-gene infection genetics and coevolutionary dynamics. The American Naturalist, 174, E230–E242.Google Scholar
Fitzpatrick, U., Murray, T.E., Paxton, R.J., et al. (2007) Rarity and decline in bumblebees – a test of causes and correlates in the Irish fauna. Biological Conservation, 136, 185–194.Google Scholar
Flegontov, P., Butenko, A., Firsov, S., et al. (2015). Genome of Leptomonas pyrrhocoris: a high-quality reference for monoxenous trypanosomatids and new insights into evolution of Leishmania. Scientific Reports, 6, 23704.Google Scholar
Folly, A.J., Koch, H., Stevenson, P.C. & Brown, M.J.F. (2017) Larvae act as a transient transmission hub for the prevalent bumblebee parasite Crithidia bombi. Journal of Invertebrate Pathology, 148, 81–85.Google Scholar
Fouks, B. & Lattorff, H.M.G. (2011) Recognition and avoidance of contaminated flowers by foraging bumblebees (Bombus terrestris). PLoS ONE, 6, e26328.Google Scholar
Frank, S.A. (1994) Coevolutionary genetics of hosts and parasites with quantitative inheritance. Evolutionary Ecology, 8, 74–94.Google Scholar
Frank, S.A. & Schmid-Hempel, P. (2008) Mechanisms of pathogenesis and the evolution of parasite virulence. Journal of Evolutionary Biology, 21, 396–404.Google Scholar
Fürst, M.A., McMahon, D.P., Osborne, J.L., Paxton, R.J. & Brown, M.J.F. (2014) Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature, 506, 364–366.Google Scholar
Gallot-Lavallée, M., Schmid-Hempel, R., Vandamme, R., Vergara, C.H. & Schmid-Hempel, P. (2016) Large scale patterns of abundance and distribution of parasites in Mexican bumblebees. Journal of Invertebrate Pathology, 133, 73–83.Google Scholar
Gandon, S. & Michalakis, Y. (2002) Local adaptation, evolutionary potential and host–parasite coevolution: interactions between migration, mutation, population size and generation time. Journal of Evolutionary Biology, 15, 451–462.Google Scholar
Gaunt, M.W., Yeo, M., Frame, I.A., et al. (2003) Mechanism of genetic exchange in American trypanosomes. Nature, 421, 936–939.Google Scholar
Gegear, R.J., Otterstatter, M.C. & Thomson, J.D. (2006) Bumble-bee foragers infected by a gut parasite have an impaired ability to utilize floral information. Proceedings of the Royal Society of London B, 273, 1073–1078.Google Scholar
Gibson, W. & Stevens, J. (1999) Genetic exchange in the Trypanosomatidae. Advances in Parasitology, 43, 1–46.Google Scholar
Gillespie, S.D. & Adler, L.S. (2013) Indirect effects on mutualisms: parasitism of bumble bees and pollination service to plants. Ecology, 94, 454–464.Google Scholar
Gillespie, S.D., Carrero, K. & Adler, L.S. (2015) Relationships between parasitism, bumblebee foraging behaviour, and pollination service to Trifolium pratense flowers. Ecological Entomology, 40, 650–653.CrossRefGoogle Scholar
Goulson, D. (2003a) Bumblebees – Their Behaviour and Ecology. New York, NY: Oxford University Press.Google Scholar
Goulson, D. (2003b) Conserving wild bees for crop pollination. Food, Agriculture & Environment, 1, 142–144.Google Scholar
Goulson, D., Lye, G.C. & Darvill, B. (2008) Decline and conservation of bumble bees. Annual Review of Ecology and Systematics, 53, 191–208.Google Scholar
Graystock, P., Goulson, D. & Hughes, W.O.H. (2015) Parasites in bloom: flowers aid dispersal and transmission of pollinator parasites within and between bee species. Proceedings of the Royal Society of London B, 282.Google Scholar
Hamilton, W.D. (1980) Sex versus non-sex versus parasite. Oikos, 35, 282–290.Google Scholar
Hamilton, W.D., Axelrod, A. & Tanese, R. (1990) Sexual reproduction as an adaptation to resist parasites (a review). Proceedings of the National Academy of Sciences of the United States of America, 87, 3566–3573.Google Scholar
Hamilton, W.D. & Zuk, M. (1982) Heritable true fitness and bright birds: a role for parasites? Science, 218, 384–387.Google Scholar
Howard, R.S. & Lively, C.M. (2002) The Ratchet and the Red Queen: the maintenance of sex in parasites. Journal of Evolutionary Biology, 15, 648–656.CrossRefGoogle Scholar
Imhoof, B. & Schmid-Hempel, P. (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.Google Scholar
Inoue, M.N., Yokoyama, J. & Tsuchida, K. (2010) Colony growth and reproductive ability of feral nests of the introduced bumblebee Bombus terrestris in northern Japan. Insectes Sociaux, 57, 29–38.Google Scholar
Ishemgulova, A., Butenko, A., Kortisiova, L., et al. (2017) Molecular mechanisms of thermal resistance of the insect trypanosomatid Crithidia thermophila. PLoS ONE, 12, e0174165.Google Scholar
Koch, H., Abrol, D.P., Li, J. & Schmid-Hempel, P. (2013) Diversity and possible evolutionary patterns of bacterial gut associates of corbiculate bees. Molecular Ecology, 22, 2028–2044.CrossRefGoogle Scholar
Koch, H. & Schmid-Hempel, P. (2011a) Bacterial communities in Central European bumblebees: low diversity and high specificity. Microbial Ecology, 62, 121–133.CrossRefGoogle ScholarPubMed
Koch, H. & Schmid-Hempel, P. (2011b) Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proceedings of the National Academy of Sciences of the United States of America, 108, 19,288–19,292.Google Scholar
Koch, H. & Schmid-Hempel, P. (2012) Gut microbiota instead of host genotype drive the specificity in the interaction of a natural host–parasite system. Ecology Letters, 15, 1095–1103.CrossRefGoogle ScholarPubMed
König, C. & Schmid-Hempel, P. (1995) Foraging activity and immunocompetence in workers of the bumble bee, Bombus terrestris L. Proceedings of the Royal Society of London B, 260, 225–227.Google Scholar
Korner, P. & Schmid-Hempel, P. (2004) In vivo dynamics of an immune response in the bumble bee Bombus terrestris. Journal of Invertebrate Pathology, 87, 59–66.CrossRefGoogle ScholarPubMed
Kwong, W.K., Engel, P., Koch, H. & Moran, N.A. (2014) Genomics and host specialization of honey bee and bumble bee gut symbionts. Proceedings of the National Academy of Sciences of the United States of America, 111, 11,509–11,514.Google Scholar
Leggett, H.C., Cornwallis, C.K. & West, S.A. (2012) Mechanisms of pathogenesis, infective dose and virulence in human parasites. PLoS Pathogens, 8, e1002512.Google Scholar
Lemaitre, B. (2012) The drosophila gut: a new paradigm for epithelial immune response. Cytokine, 59, 494.Google Scholar
Ley, R.E., Lozupone, C.A., Hamady, M., Knight, R. & Gordon, J.I. (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nature Reviews Microbiology, 6, 776–788.Google Scholar
Li, J., Chen, W., Wu, J., et al. (2012) Diversity of Nosema associated with bumblebees (Bombus spp.) from China. International Journal of Parasitology, 42, 49–61.Google Scholar
Little, T.J. & Kraaijeveld, A.R. (2004) Ecological and evolutionary implications of immunological priming in invertebrates. Trends in Ecology and Evolution, 19, 58–60.Google Scholar
Luijckx, P., Fienberg, H., Duneau, D. & Ebert, D. (2013) A matching-allele model explains host resistance to parasites. Current Biology, 23, 1–4.Google Scholar
MacLeod, A., Tweedie, A., McLellan, S., et al. (2005) Allelic segregation and independent assortment in Trypanosoma brucei crosses: proof that the genetic system is Mendelian and involves meiosis. Molecular and Biochemical Parasitology, 143, 12–19.Google Scholar
Maharramov, J., Meeus, I., Maebe, K., et al. (2013) Genetic variability of the Neogregarine Apicystis bombi, an etiological agent of an emergent bumblebee disease. PLoS ONE, 8, e81475.Google Scholar
Manley, R., Boots, M. & Bayer-Wilfert, L. (2017) Condition-dependent virulence of Slow Bee Paralysis Virus in Bombus terrestris: are the impacts of honeybee viruses in wild pollinators underestimated? Oecologia, 184, 305–315.CrossRefGoogle ScholarPubMed
Martinez-Calvillo, S., Vizuet-de-Rueda, J.C., Florencio-Martinez, L.E., Manning-Cela, R.G. & Figuera-Angulo, E.E. (2010) Gene expression in trypanosomatid parasites. Journal of Biomedicine and Biotechnology, 2010, 525241.Google Scholar
Martinson, V.G., Danforth, B.N., Minckley, R.L., et al. (2011) A simple and distinctive microbiota associated with honey bees and bumble bees. Molecular Ecology, 20, 619–628.Google Scholar
Marxer, M., Barribeau, S.M. & Schmid-Hempel, P. (2016a) Experimental evolution of a trypanosome parasite of bumblebees and its implications for infection success and host immune response. Evolutionary Biology, 43, 160–170.Google Scholar
Marxer, M., Vollenweider, V. & Schmid-Hempel, P. (2016b) Insect antimicrobial peptides act synergistically to inhibit a trypanosome parasite. Philosophical Transactions of the Royal Society B, 371, 20150302.Google Scholar
McArt, S.H., Koch, H., Irwin, R.E. & Adler, L.S. (2014) Arranging the bouquet of disease: floral traits and the transmission of plant and animal pathogens. Ecology Letters, 17, 624–636.Google Scholar
McMahon, D., Fürst, M., Caspar, J., et al. (2015) A sting in the spit: widespread cross-infection of multiple RNA viruses across wild and managed bees. Journal of Animal Ecology, 84, 615–624.Google Scholar
Mikaelyan, A., Thompson, C.L., Hofer, M.J. & Brune, A. (2015) Deterministic assembly of complex bacterial communities in guts of germ-free cockroaches. Applied and Environmental Microbiology, 82, 1256–1263.CrossRefGoogle ScholarPubMed
Mikkola, K. (1984) Migration of wasp and bumble bee queens across the Gulf of Finland (Hymenoptera: Vespidae and Apidae). Notulae Entomologica, 64, 125–128.Google Scholar
Moore, J. (1984) Parasites and altered host behavior. Scientific American, 250, 108–115.Google Scholar
Moran, N.A., Hansen, A.K., Powell, J.E. & Sabree, Z.L. (2012) Distinctive gut microbiota of honey bees assessed using deep sampling from individual worker bees. PLoS ONE, 7, e36393.Google Scholar
Moret, Y. & Schmid-Hempel, P. (2000) Survival for immunity: the price of immune system activation for bumblebee workers. Science, 290, 1166–1168.Google Scholar
Müller, C.B. & Schmid-Hempel, P. (1993) Correlates of reproductive success among field colonies of Bombus lucorum L.: the importance of growth and parasites. Ecological Entomology, 17, 343–353.Google Scholar
Näpflin, K. & Schmid-Hempel, P. (2018) Host effects on microbiota community assembly. Journal of Animal Ecology, 87, 331–340.Google Scholar
Näpflin, K. & Schmid-Hempel, P. (2018) High gut microbiota diversity provides lower resistance against infection by an intestinal parasite. American Naturalist, 192, 131–141.Google Scholar
Otterstatter, M.C., Gegear, R.J., Colla, S. & Thomson, J.D. (2005) Effects of parasitic mites and protozoa on the flower constancy and foraging rate of bumble bees. Behavioural Ecology and Scoiobiology, 58, 383–389.Google Scholar
Peters, A.D. & Lively, C.M. (1999) The Red Queen and fluctuating epistasis: a population genetic analysis of antagonistic coevolution. The American Naturalist, 154, 393–405.Google Scholar
Råberg, L., Sim, D. & Read, A.F. (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science, 318, 812–814.CrossRefGoogle ScholarPubMed
Rahnamaeian, M., Cytryńska, M., Zdybicka-Barabas, A., et al. (2015) Insect antimicrobial peptides show potentiating functional interactions against Gram-negative bacteria. Proceedings of the Royal Society of London B, 282, 20150293.Google Scholar
Ravoet, J., Schwarz, R.S., Descamps, T., et al. (2015) Differential diagnosis of the honey bee trypanosomatids Crithidia mellificae and Lotmaria passim. Journal of Invertebrate Pathology, 130, 21–27.Google Scholar
Rheins, L.A. & Karp, R.D. (1986) Effect of gender on the inducible humoral immune response to honeybee venom in the American cockroach (Periplaneta americana). Developmental and Comparative Immunology, 9, 41–49.Google Scholar
Richardson, L.L., Adler, L.S., Leonard, A.S., et al. (2015) Secondary metabolites in floral nectar reduce parasite infections in bumblebees. Proceedings of the Royal Society of London B, 282, 20142471.Google Scholar
Richardson, L.L., Bowers, M.D. & Irwin, R.E. (2016) Nectar chemistry mediates the behavior of parasitized bees: consequences for plant fitness. Ecology, 97, 325–337.Google Scholar
Riddell, C., Adams, S., Schmid-Hempel, P., Mallon, E.B. & Rankin, D.J. (2009). Differential expression of immune defences is associated with specific host–parasite interactions in insects. PLoS ONE, 4, e7621.Google Scholar
Riddell, C.E., Lobaton Garces, J.D., Adams, S., et al. (2014) Differential gene expression and alternative splicing in insect immune specificity. BMC Genomics, 15, 1031.Google Scholar
Riddell, C.E., Sumner, S., Adams, S. & Mallon, E.B. (2011) Pathways to immunity: temporal dynamics of the bumblebee (Bombus terrestris) immune response against a trypanosome gut parasite. Insect Molecular Biology, 20, 529–540.Google Scholar
Routtu, J. & Ebert, D. (2015) Genetic architecture of resistance in Daphnia hosts against two species of host-specific parasites. Heredity, 114, 241–248.Google Scholar
Ruiz-Gonzalez, M.X., Bryden, J., Moret, Y., et al. (2012) Dynamic transmission, host quality and population structure in a multi-host parasite of bumble bees. Evolution, 66, 3052–3066.Google Scholar
Sadd, B., Kleinlogel, Y., Schmid-Hempel, R. & Schmid-Hempel, P. (2005) Trans-generational immune priming in a social insect. Biology Letters, 1, 386–388.Google Scholar
Sadd, B. & Schmid-Hempel, P. (2006) Insect immunity shows specificity in protection upon secondary pathogen exposure. Current Biology, 16, 1206–1210.Google Scholar
Sadd, B. & Schmid-Hempel, P. (2007) Facultative but persistent trans-generational immunity via the mother’s eggs in bumblebees. Current Biology, 17, R1046–R1047.Google Scholar
Sadd, B. & Schmid-Hempel, P. (2009) A distinct infection cost associated with trans-generational immune priming of antibacterial immunity in bumble-bees. Biology Letters, 5, 798–801.Google Scholar
Sadd, B.M., Barribeau, S.M., Bloch, G., et al. (2015) The genomes of two key bumblebee species with primitive eusocial organization. Genome Biology, 16, 76.Google Scholar
Salathé, M., Kouyos, R.D. & Bonhoeffer, S. (2008) The state of affairs in the kingdom of the Red Queen. Trends in Ecology and Evolution, 23, 439–445.Google Scholar
Salathé, R. & Schmid-Hempel, P. (2011) Genotypic structure of a multi-host bumblebee parasite suggests a major role for ecological niche overlap. PLoS ONE, 6, e22054.Google Scholar
Salathé, R. & Schmid-Hempel, P. (2012) Probing mixed-genotype infections I: extraction and cloning of infections from hosts of the trypanosomatid Crithidia bombi. PLoS ONE, 7, e49046.Google Scholar
Sasaki, A. (2000) Host–parasite coevolution in a multilocus gene-for-gene system. Proceedings of the Royal Society of London B, 267, 2183–2188.Google Scholar
Sauter, A., Brown, M.J.F., Baer, B. & Schmid-Hempel, P. (2001) Males of social insects can prevent queens from multiple mating. Proceedings of the Royal Society of London B, 268, 1449–1454.Google Scholar
Schaub, G.A. (1992) The effects of trypanosomatids on insects. Advances in Parasitology, 31, 255–319.CrossRefGoogle ScholarPubMed
Schlüns, H., Sadd, B.M., Schmid-Hempel, P. & Crozier, R.H. (2010). Infection with the trypanosome Crithidia bombi and expression of immune-related genes in the bumblebee Bombus terrestris. Developmental and Comparative Immunology, 34, 705–709.Google Scholar
Schmid-Hempel, P. (1998) Parasites in Social Insects. Princeton, NJ: Princeton University Press.Google Scholar
Schmid-Hempel, P. (2001) On the evolutionary ecology of host–parasite interactions – addressing the questions with bumblebees and their parasites. Naturwissenschaften, 88, 147–158.Google Scholar
Schmid-Hempel, P. (2003) Variation in immune defence as a question of evolutionary ecology. Proceedings of the Royal Society of London B, 270, 357–366.CrossRefGoogle ScholarPubMed
Schmid-Hempel, P. (2005) Natural insect host–parasite systems show immune priming and specificity – puzzles to be solved. BioEssays, 27, 1026–1034.Google Scholar
Schmid-Hempel, P. (2011) Evolutionary Parasitology – The Integrated Study of Infections, Immunology, Ecology, and Genetics. Oxford: Oxford University Press.Google Scholar
Schmid-Hempel, P. (2017) Parasites and their social hosts. Trends in Parasitology, 33, 453–462.CrossRefGoogle ScholarPubMed
Schmid-Hempel, P., Aebi, M., Barribeau, S., et al. (2018) The genomes of Crithidia bombi and C. expoeki, common parasites of bumblebees. PLoS ONE, 13(1), e0189738.Google Scholar
Schmid-Hempel, P. & Frank, S.A. (2007) Pathogenesis, virulence, and infective dose. PLoS Pathogens, 3, 1372–1373.Google Scholar
Schmid-Hempel, P., Puhr, K., Kruger, N., Reber, C. & Schmid-Hempel, R. (1999) Dynamic and genetic consequences of variation in horizontal transmission for a microparasitic infection. Evolution, 53, 426–434.Google Scholar
Schmid-Hempel, P. & Reber Funk, C. (2004) The distribution of genotypes of the trypanosome parasite, Crithidia bombi, in populations of its host, Bombus terrestris.Parasitology, 129, 147–158.Google Scholar
Schmid-Hempel, P. & Schmid-Hempel, R. (1993) Transmission of a pathogen in Bombus terrestris, with a note on division of labour in social insects. Behavioural Ecology and Sociobiology, 33, 319–327.Google Scholar
Schmid-Hempel, P. & Stauffer, H.P. (1998). Parasites and flower choice of bumblebees. Animal Behaviour, 55, 819–825.Google Scholar
Schmid-Hempel, R., Eckhardt, M., Goulson, D., et al. (2013) The invasion of southern South America by imported bumblebees and associated parasites. Journal of Animal Ecology, 83, 823–837.Google Scholar
Schmid-Hempel, R. & Schmid-Hempel, P. (2000) Female mating frequencies in social insects: Bombus spp. from Central Europe. Insectes Sociaux, 47, 36–41.Google Scholar
Schmid-Hempel, R. & Tognazzo, M. (2010) Molecular divergence defines two distinct lineages of Crithidia bombi (Trypanosomatidae), parasites of bumblebees. Journal of Eukaryotic Microbiology, 57, 337–345.Google Scholar
Schmid-Hempel, R., Tognazzo, M., Salathé, R. & Schmid-Hempel, P. (2011) Genetic exchange and emergence of novel strains in directly transmitted trypanosomatids. Infection, Genetics, and Evolution, 11, 564–571.Google Scholar
Schwarz, R.S., Bauchan, G., Murphy, C., et al. (2015) Characterization of two species of Trypanosomatidae from the honey bee Apis mellifera: Crithidia mellificae Langridge and McGhee, 1967 and Lotmaria passim n. gen., n. sp. Journal of Eukaryotic Microbiology, 62, 567–583.Google Scholar
Schwarz, R.S. & Evans, J.D. (2013) Single and mixed-species trypanosome and microsporidia infections elicit distinct, ephemeral cellular and humoral immune responses in honey bees. Developmental & Comparative Immunology, 40, 300–310.Google Scholar
Shykoff, J.A. & Schmid-Hempel, P. (1991) Parasites delay worker reproduction in bumblebees: consequences for eusociality. Behavioral Ecology, 2, 242–248.Google Scholar
Simpson, A., Stevens, J. & Lukes, J. (2006) The evolution and diversity of kinetoplastid flagellates. Trends in Parasitology, 22, 168–174.Google Scholar
Stout, J.C. & Goulson, D. (2001) The use of conspecific and interspecific scent marks by foraging bumblebees and honeybees. Animal Behaviour, 62, 183–189.Google Scholar
Tait, A., Morrison, L.J., Duffy, C.W., et al. (2011). Trypanosome genetics: populations, phenotypes and diversity. Veterinary Parasitology, 181, 61–68.Google Scholar
Tibayrenc, M. & Ayala, F.J. (2002) The clonal theory of parasitic protozoa: 12 years on. Trends in Parasitology, 18, 405–410.Google Scholar
Tibayrenc, M. & Ayala, F.J. (2013) How clonal are Trypanosoma and Leishmania? Trends in Parasitology, 29, 264–269.Google Scholar
Tognazzo, M., Schmid-Hempel, R. & Schmid-Hempel, P. (2012) Probing mixed-genotype infections II: high multiplicity in natural infections of the trypanosomatid, Crithidia bombi, in its host, Bombus spp. PLoS ONE, 7, e49137.Google Scholar
Ulrich, Y., Sadd, B. & Schmid-Hempel, P. (2011) Strain filtering and transmission of a mixed infection in a social insect. Journal of Evolutionary Biology, 24, 354–362.Google Scholar
Ulrich, Y. & Schmid-Hempel, P. (2012) Host modulation of parasite competition in multiple infections. Proceedings of the Royal Society of London B, 279, 2982–2989.Google Scholar
Ulrich, Y. & Schmid-Hempel, P. (2015) The distribution of parasite strains among hosts affects disease spread in a social insect. Infection, Genetics, Evolution, 32, 348–353.Google Scholar
Van Boven, M. & Weissing, F.J. (2004) The evolutionary economics of immunity. The American Naturalist, 163, 277–294.Google Scholar
Velthuis, H.H.W. & van Doorn, A. (2006) A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie, 37, 421–451.Google Scholar
Widmer, A. & Schmid-Hempel, P. (1999) The population genetic structure of a large temperate pollinator species, Bombus pascuorum (Scopoli) (Hymenoptera, Apidae). Molecular Ecology, 8, 387–398.Google Scholar
Widmer, A., Schmid-Hempel, P., Estoup, A. & Scholl, A. (1998) Population genetic structure and colonization history of Bombus terrestris s.l. (Hymenoptera: Apidae) from the Canary Islands and Madeira. Heredity, 81, 563–572.Google Scholar
Wilfert, L., Gadau, J., Baer, B. & Schmid-Hempel, P. (2007) Natural variation in the genetic architecture of a host–parasite interaction in the bumblebee, Bombus terrestris.Molecular Ecology, 16, 1327–1339.Google Scholar
Williams, P.H., Brown, M.J.F., Carolan, J.C., et al. (2012) Assessing cryptic species of the bumblebee subgenus Bombus s. str. world-wide with COI barcodes (Hymenoptera: Apidae). Systematics and Biodiversity, 10, 21–56.Google Scholar
Williams, P.H., Cameron, S.A., Hines, H.M., Cederbergc, B. & Rasmont, P. (2008) A simplified subgeneric classification of the bumblebees (genus Bombus). Apidologie, 39, 1–29.Google Scholar
Wilson, K., Thomas, M.B., Blanford, S., et al. (2002) Coping with crowds: density-dependent disease resistance in desert locusts. Proceedings of the National Academy of Sciences of the United States of America, 99, 5471–5475.CrossRefGoogle ScholarPubMed
Yourth, C.P. (2004) Virulence and transmission of Crithidia bombi in bumble bees. PhD thesis, ETH Zurich. Zurich: ETH Zurich.Google Scholar
Yourth, C.P. & Schmid-Hempel, P. (2006) Serial passage of the parasite Crithidia bombi within a colony of its host, Bombus terrestris, reduces success in unrelated hosts. Proceedings of the Royal Society of London B, 273, 655–659.Google ScholarPubMed
Zasloff, M. (2013) Antimicrobial Peptides. New York, NY: John Wiley & Son.Google Scholar
Zuk, M.& Stoehr, A.M. (2002) Immune defence and host life history. American Naturalist, 160, S9–S22.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×