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Horizontal transmission of a parasite is influenced by infected host phenotype and density

Published online by Cambridge University Press:  11 August 2014

K. E. ROBERTS*
Affiliation:
School of Biology, University of Leeds, Leeds LS2 9JT, UK
W. O. H. HUGHES
Affiliation:
School of Life Sciences, University of Sussex, Brighton BN1 9QG, UK
*
*Corresponding author: School of Biology, University of Leeds, Leeds LS2 9JT, UK. E-mail: k.roberts@exeter.ac.uk

Summary

Transmission is a key determinant of parasite fitness, and understanding the dynamics of transmission is fundamental to the ecology and evolution of host–parasite interactions. Successful transmission is often reliant on contact between infected individuals and susceptible hosts. The social insects consist of aggregated groups of genetically similar hosts, making them particularly vulnerable to parasite transmission. Here we investigate how the ratio of infected to susceptible individuals impacts parasite transmission, using the honey bee, Apis mellifera and its microsporidian parasite Nosema ceranae. We used 2 types of infected hosts found simultaneously in colonies; sterile female workers and sexual males. We found a higher ratio of infected to susceptible individuals in groups resulted in a greater proportion of susceptibles becoming infected, but this effect was non-linear and interestingly, the ratio also affected the spore production of infected individuals. The transmission level was much greater in an experiment where the infected individuals were drones than in an experiment where they were workers, suggesting drones may act as intracolonial ‘superspreaders’. Understanding the subtleties of transmission and how it is influenced by the phenotype of the infected/susceptible individuals is important for understanding pathogen transmission at population level, and for optimum targeting of parasite control strategies.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Anderson, R. M. and May, R. M. (1981). The population dynamics of microparasites and their invertebrate hosts. Philosophical Transactions of the Royal Society of London Biological Sciences 291, 451524. doi: 10.1098/rstb.1981.0005.Google Scholar
Anderson, R. M. and May, R. M. (1982). Coevolution of hosts and parasites. Parasitology 85, 411426.Google Scholar
Armitage, S. A. O. and Boomsma, J. J. (2010). The effects of age and social interactions on innate immunity in a leaf-cutting ant. Journal of Insect Physiology 56, 780787. doi: 10.1016/j.jinsphys.2010.01.009.Google Scholar
Baer, B. and Schmid-Hempel, P. (2003). Bumblebee workers from different sire groups vary in susceptibility to parasite infection. Ecology Letters 6, 106110. doi: 10.1046/j.1461-0248.2003.00411.x.Google Scholar
Baer, B., Krug, A., Boomsma, J. J. and Hughes, W. O. H. (2005). Examination of the immune responses of males and workers of the leaf-cutting ant Acromyrmex echinatior and the effect of infection. Insectes Sociaux 52, 298303. doi: 10.1007/s00040-005-0809-x.Google Scholar
Bateman, A. (1948). Intra sexual selection in Drosophila . Heredity 2, 349368. doi: 10.1038/hdy.1948.21.Google Scholar
Bates, D. and Maechler, M. (2010). lme4: linear mixed-effects models using S4 classes. R package version 0.999375–33.Google Scholar
Begon, M., Bennett, M., Bowers, R. G., French, N. P., Hazel, S. M. and Turner, J. (2002). A clarification of transmission terms in host–microparasite models: numbers, densities and areas. Epidemiology and Infection 129, 147153. doi: 10.1017/S0950268802007148.Google Scholar
Boomsma, J. J., Schmid-Hempel, P. and Hughes, W. O. H. (2005). Life histories and parasite pressure across the major groups of social insects. In Insect Evolutionary Ecology (ed. Fellowes, M. D. E., Holloway, G. J. and Rolff, J.), pp. 139176. CABI Publishing, London.Google ScholarPubMed
Boot, W. J., Schoenmaker, J., Calis, J. N. M. and Beetsma, J. (1995). Invasion of Varroa jacobsoni into drone brood cells of the honey bee, Apis mellifera . Apidologie 26, 109118. doi: 10.1051/apido:19950204.CrossRefGoogle Scholar
Botías, C., Martín-Hernández, R., Días, J., García-Palencia, P., Matabuena, M., Juarranz, A., Barrios, L., Meana, A., Nanetti, A. and Higes, M. (2012). The effect of induced queen replacement on Nosema spp. infection in honey bee (Apis mellifera iberiensis) colonies. Environmental Microbiology 14, 845859. doi: 10.1111/j.1462-2920.2011.02647.x.CrossRefGoogle ScholarPubMed
Chen, Y. P., Evans, J. D., Smith, I. B. and Pettis, J. S. (2008). Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States. Journal of Invertebrate Pathology 97, 186188. doi: 10.1016/j.jip.2007.07.010.CrossRefGoogle ScholarPubMed
Chen, Y. P., Evans, J. D., Murphy, C., Gutell, R., Zuker, M., Gundensen-Rindal, D. and Pettis, J. S. S. (2009). Morphological, molecular, and phylogenetic characterization of Nosema ceranae, a microsporidian parasite isolated from the European honey bee, Apis mellifera . The Journal of Eukaryotic Microbiology 56, 142147. doi: 10.1111/j.1550-7408.2008.00374.x.CrossRefGoogle ScholarPubMed
Cornman, R. S., Chen, Y., Schatz, M. C., Street, C., Zhao, Y., Desany, B., Egholm, M., Hutchison, S., Pettis, J. S., Lipkin, W. I. and Evans, J. D. (2009). Genomic analyses of the microsporidian Nosema ceranae, an emergent pathogen of honey bees. PLoS Pathogens 5, e1000466. doi: 10.1371/journal.ppat.1000466.Google Scholar
Cotter, S. C. and Kilner, R. M. (2010). Personal immunity versus social immunity. Behavioral Ecology 21, 663668. doi: 10.1093/beheco/arq070.CrossRefGoogle Scholar
Crailsheim, K. (1988). Regulation of food passage in the intestine of the honeybee. Journal of Insect Physiology 34, 8590. doi: 10.1016/0022-1910(88)90158-8.CrossRefGoogle Scholar
Cremer, S., Armitage, S. A. O. and Schmid-Hempel, P. (2007). Social immunity. Current Biology 17, R693. doi: 10.1016/j.cub.2007.06.008.CrossRefGoogle ScholarPubMed
De Jong, M. C. M. (1995). Mathematical modelling in veterinary epidemiology: why model building is important. Preventive Veterinary Medicine 25, 183193. doi: 10.1016/0167-5877(95)00538-2.CrossRefGoogle Scholar
De Miranda, J. R. and Fries, I. (2008). Venereal and vertical transmission of deformed wing virus in honeybees (Apis mellifera L.). Journal of Invertebrate Pathology 98, 184189. doi: 10.1016/j.jip.2008.02.004.CrossRefGoogle ScholarPubMed
Feigenbaum, C. and Naug, D. (2010). The influence of social hunger on food distribution and its implications for disease transmission in a honeybee colony. Insectes Sociaux 57, 217222. doi: 10.1007/s00040-010-0073-6.CrossRefGoogle Scholar
Fenton, A., Fairbairn, J. P., Norman, R. and Hudson, P. J. (2002). Parasite transmission: reconciling theory and reality. Journal of Animal Ecology 71, 893905.CrossRefGoogle Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294299.Google Scholar
Forsgren, E. and Fries, I. (2010). Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Veterinary Parasitology 170, 212217. doi: 10.1016/j.vetpar.2010.02.010.CrossRefGoogle ScholarPubMed
Freeland, W. J. (1976). Pathogens and the evolution of primate sociality. Biotropica 8, 1224.Google Scholar
Fries, I. (2010). Nosema ceranae in European honey bees (Apis mellifera). Journal of Invertebrate Pathology 103(Suppl.), S73S79. doi: 10.1016/j.jip.2009.06.017.Google Scholar
Fuchs, S. (1990). Preference for drone brood cells by Varroa jacobsoni Oud in colonies of Apis mellifera carnica . Apidologie 21, 193199. doi: 10.1051/apido:19900304.CrossRefGoogle Scholar
Galvani, A. P. and May, R. M. (2005). NEWS and VIEWS dimensions of superspreading. Nature 438, 293295. doi: 10.1038/438293a.CrossRefGoogle Scholar
Gisder, S. and Genersch, E. (2013). Molecular differentiation of Nosema apis and Nosema ceranae based on species-specific sequence differences in a protein coding gene. Journal of Invertebrate Pathology 113, 16. doi: 10.1016/j.jip.2013.01.004.Google Scholar
Grear, D. A., Luong, L. T. and Hudson, P. J. (2012). Sex-biased transmission of a complex life-cycle parasite: why males matter. Oikos 121, 14461453. doi: 10.1111/j.1600-0706.2012.20358.x.Google Scholar
Hawley, D. M. and Altizer, S. M. (2011). Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Functional Ecology 25, 4860. doi: 10.1111/j.1365-2435.2010.01753.x.Google Scholar
Higes, M., Martin-Hernandez, R., Aránzazu, M., Martín, R. and Meana, A. (2006). Nosema ceranae, a new microsporidian parasite in honeybees in Europe. Journal of Invertebrate Pathology 92, 9395. doi: 10.1016/j.jip.2006.02.005.Google Scholar
Higes, M., García-Palencia, P., Martín-Hernández, R. and Meana, A. (2007). Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). Journal of Invertebrate Pathology 94, 211.Google Scholar
Higes, M., Martín-Hernández, R., Botías, C., Bailón, E. G., González-Porto, A. V., Barrios, L., del Nozal, M. J., Bernal, J. L., Jiménez, J. J. and Palencia, P. G. (2008). How natural infection by Nosema ceranae causes honeybee colony collapse. Environmental Microbiology 10, 26592669. doi: 10.1111/j.1462-2920.2008.01687.x.Google Scholar
Higes, M., Martín-Hernández, R., Garrido-Bailón, E., González-Porto, A. V., García-Palencia, P., Meana, A., Del Nozal, M. J., Mayo, R. and Bernal, J. L. (2009). Honeybee colony collapse due to Nosema ceranae in professional apiaries. Environmental Microbiology Reports 1, 110113. doi: 10.1111/j.1758-2229.2009.00014.x.Google Scholar
Huang, W., Jiang, J.-H. J., Chen, Y.-W. and Wang, C.-H. (2007). A Nosema ceranae isolate from the honeybee Apis mellifera . Apidologie 38, 3037. doi: 10.1051/apido.Google Scholar
Huang, W.-F. and Solter, L. F. (2013). Comparative development and tissue tropism in Nosema apis and Nosema ceranae . Journal of Invertebrate Pathology 113, 3541. doi: 10.1016/j.jip.2013.01.001.Google Scholar
Hughes, W. O. H., Eilenberg, J. and Boomsma, J. J. (2002). Trade-offs in group living: transmission and disease resistance in leaf-cutting ants. Proceedings of the Royal Society B: Biological Sciences 269, 18111819. doi: 10.1098/rspb.2002.2113.CrossRefGoogle ScholarPubMed
Hughes, W. O. H., Petersen, K. S., Ugelvig, L. V., Pedersen, D., Thomsen, L., Poulsen, M. and Boomsma, J. J. (2004). Density-dependence and within-host competition in a semelparous parasite of leaf-cutting ants. BMC Evolutionary Biology 4, 45. doi: 10.1186/1471-2148-4-45.Google Scholar
Hughes, W. O. H., Bot, A. N. M. and Boomsma, J. J. (2010). Caste-specific expression of genetic variation in the size of antibiotic-producing glands of leaf-cutting ants. Proceedings Biological Sciences/The Royal Society 277, 609615. doi: 10.1098/rspb.2009.1415.CrossRefGoogle ScholarPubMed
Johnson, M. B., Lafferty, K. D., van Oosterhout, C. and Cable, J. (2011). Parasite transmission in social interacting hosts: monogenean epidemics in guppies. PloS ONE 6, e22634. doi: 10.1371/journal.pone.0022634.Google Scholar
Klee, J., Besana, A. M., Genersch, E., Gisder, S., Nanetti, A., Tam, D. Q., Chinh, T. X., Puerta, F., Ruz, J. M., Kryger, P., Message, D., Hatjina, F., Korpela, S., Fries, I. and Paxton, R. J. (2007). Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera . Journal of Invertebrate Pathology 96, 1. doi: 10.1016/j.jip.2007.02.014.CrossRefGoogle ScholarPubMed
Knell, R. J., Begon, M. and Thompson, D. J. (1996). Transmission dynamics of Bacillus thuringiensis infecting Plodia interpunctella: a test of the mass action assumption with an insect pathogen. Proceedings Biological Sciences/The Royal Society 263, 7581. doi: 10.1098/rspb.1996.0013.Google Scholar
Knell, R. J., Begon, M. and Thompson, D. J. (1998). Transmission of Plodia interpunctella granulosis virus does not conform to the mass action model. Journal of Animal Ecology 67, 592599. doi: 10.1046/j.1365-2656.1998.00219.x.Google Scholar
Lloyd-Smith, J. O., Schreiber, S. J., Kopp, P. E. and Getz, W. M. (2005). Superspreading and the effect of individual variation on disease emergence. Nature 438, 355359. doi: 10.1038/nature04153.Google Scholar
Martin-Hernandez, R., Meana, A., Garcia-Palencia, P., Marin, P., Botias, C., Garrido-Bailon, E., Barrios, L. and Higes, M. (2009). Effect of temperature on the biotic potential of honeybee microsporidia. Applied and Environmental Microbiology 75, 25542557. doi: 10.1128/aem.02908-08.Google Scholar
Matthews, L., Reeve, R., Woolhouse, M. E. J., Chase-Topping, M., Mellor, D. J., Pearce, M. C., Allison, L. J., Gunn, G. J., Low, J. C. and Reid, S. W. J. (2009). Exploiting strain diversity to expose transmission heterogeneities and predict the impact of targeting supershedding. Epidemics 1, 221229. doi: 10.1016/j.epidem.2009.10.002.Google Scholar
Mayack, C. and Naug, D. (2009). Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. Journal of Invertebrate Pathology 100, 185188. doi: 10.1016/j.jip.2008.12.001.Google Scholar
McCallum, H., Barlow, N. and Hone, J. (2001). How should pathogen transmission be modelled? Trends in Ecology and Evolution 16, 295300. doi: http://dx.doi.org/10.1016/S0169-5347(01)02144-9.CrossRefGoogle ScholarPubMed
McCallum, H., Barlow, N. and Hone, J. (2002). Modelling transmission: mass action and beyond. Trends in Ecology and Evolution 17, 6465. doi: 10.1016/S0169-5347(01)02399-0.CrossRefGoogle Scholar
Moore, J. (1995). The behavior of parasitized animals when an ant…is not an ant. BioScience 45, 8996.Google Scholar
Naug, D. and Camazine, S. (2002). The role of colony organization on pathogen transmission in social insects. Journal of Theoretical Biology 215, 427439. doi: 10.1006/jtbi.2001.2524.CrossRefGoogle ScholarPubMed
Naug, D. and Gibbs, A. (2009). Behavioral changes mediated by hunger in honeybees infected with Nosema ceranae . Apidologie 40, 595599. doi: 10.1051/apido/2009039.CrossRefGoogle Scholar
Naug, D. and Smith, B. (2007). Experimentally induced change in infectious period affects transmission dynamics in a social group. Proceedings Biological Sciences/The Royal Society 274, 6165. doi: 10.1098/rspb.2006.3695.Google Scholar
Nowak, M. A. and May, R. M. (1994). Superinfection and the evolution of parasite virulence. Proceedings Biological Sciences/The Royal Society 255, 8189. doi: 10.1098/rspb.1994.0012.Google Scholar
Nunn, C. L., Lindenfors, P., Pursall, E. R. and Rolff, J. (2009). On sexual dimorphism in immune function. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 364, 6169. doi: 10.1098/rstb.2008.0148.Google Scholar
O'Donnell, S. and Beshers, S. N. (2004). The role of male disease susceptibility in the evolution of haplodiploid insect societies. Proceedings of the Royal Society B: Biological Sciences 271, 979983. doi: 10.1098/rspb.2004.2685.Google Scholar
Paxton, R. J., Klee, J., Korpela, S. and Fries, I. (2007). Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis . Apidologie 38, 558565. doi: 10.1051/apido.Google Scholar
Perkins, S. E., Cattadori, I. M., Tagliapietra, V., Rizzoli, A. P. and Hudson, P. J. (2003). Empirical evidence for key hosts in persistence of a tick-borne disease. International Journal for Parasitology 33, 909917. doi: 10.1016/S0020-7519(03)00128-0.Google Scholar
Poulsen, M., Hughes, W. O. H. and Boomsma, J. (2006). Differential resistance and the importance of antibiotic production in Acromyrmex echinatior leaf-cutting ant castes towards the entomopathogenic fungus Aspergillus nomius . Insectes Sociaux 53, 349.Google Scholar
Prendini, L., Weygoldt, P. and Wheeler, W. C. (2005). Systematics of the group of African whip spiders (Chelicerata: Amblypygi): evidence from behaviour, morphology and DNA. Organisms Diversity and Evolution 5, 203236. doi: 10.1016/j.ode.2004.12.004.Google Scholar
R Development Core Team (2012). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Richard, F.-J., Aubert, A. and Grozinger, C. M. (2008). Modulation of social interactions by immune stimulation in honey bee, Apis mellifera, workers. BMC Biology 6, 50. doi: 10.1186/1741-7007-6-50.Google Scholar
Richard, F.-J., Holt, H. L. and Grozinger, C. M. (2012). Effects of immunostimulation on social behavior, chemical communication and genome-wide gene expression in honey bee workers (Apis mellifera). BMC Genomics 13, 558. doi: 10.1186/1471-2164-13-558.Google Scholar
Roberts, K. E. and Hughes, W. O. H. (2014). Immunosenescence and resistance to parasite infection in the honey bee, Apis mellifera . Journal of Invertebrate Pathology, in press.Google Scholar
Rolff, J. (2002). Bateman's principle and immunity. Proceedings Biological Sciences/The Royal Society 269, 867872. doi: 10.1098/rspb.2002.1959.Google Scholar
Rosengaus, R. B., Traniello, J. F. A., Lefebvre, M. L. and Carlock, D. M. (2000). The social transmission of disease between adult male and female reproductives of the dampwood termite Zootermopsis angusticollis . Ethology Ecology and Evolution 12, 419433.Google Scholar
Rueppell, O., Hayworth, M. K. and Ross, N. P. (2010). Altruistic self-removal of health-compromised honey bee workers from their hive. Journal of Evolutionary Biology 23, 15381546. doi: 10.1111/j.1420-9101.2010.02022.x.CrossRefGoogle ScholarPubMed
Ruiz-González, M. X. and Brown, M. J. F. (2006). Honey bee and bumblebee trypanosomatids: specificity and potential for transmission. Ecological Entomology 31, 616622. doi: 10.1111/j.1365-2311.2006.00823.x.Google Scholar
Ryder, J., Miller, M. R., White, A., Knell, R. J. and Boots, M. (2007). Host–parasite population dynamics under combined frequency- and density-dependent transmission. Oikos 116, 20172026. doi: 10.1111/j.2007.0030-1299.15863.x.Google Scholar
Schmid-Hempel, P. (1998). Parasites in Social Insects. Princeton University Press, USA.Google Scholar
Shykoff, J. A. and Schmid-Hempel, P. (1991). Parasites and the advantage of genetic variability within social insect colonies. Proceedings of the Royal Society B: Biological Sciences 243, 5558. doi: 10.1098/rspb.1991.0009.Google Scholar
Smart, M. D. and Sheppard, W. S. (2012). Nosema ceranae in age cohorts of the western honey bee (Apis mellifera). Journal of Invertebrate Pathology 109, 148151. doi: 10.1016/j.jip.2011.09.009.Google Scholar
Smith, M. L. (2012). The honey bee parasite Nosema ceranae: transmissible via food exchange? PLoS ONE 7, e43319. doi: 10.1371/journal.pone.0043319.Google Scholar
Traniello, J. F. A., Rosengaus, R. B. and Savoie, K. (2002). The development of immunity in a social insect : evidence for the group facilitation of disease resistance. Proceedings of the National Academy of Sciences 99, 68386842. doi: 10.1073/pnas.102176599.Google Scholar
Traver, B. E. and Fell, R. D. (2011 a). Nosema ceranae in drone honey bees (Apis mellifera). Journal of Invertebrate Pathology 107, 234236. doi: 10.1016/j.jip.2011.05.016.Google Scholar
Traver, B. E. and Fell, R. D. (2011 b). Prevalence and infection intensity of Nosema in honey bee (Apis mellifera L.) colonies in Virginia. Journal of Invertebrate Pathology 107, 4349. doi: 10.1016/j.jip.2011.02.003.Google Scholar
Wilson, K., Knell, R., Boots, M. and Koch-Osborne, J. (2003). Group living and investment in immune defence: an interspecific analysis. Journal of Animal Ecology 72, 133143. doi: 10.1046/j.1365-2656.2003.00680.x.Google Scholar
Woolhouse, M. E. J., Dye, C., Etard, J. F., Smith, T., Charlwood, J. D., Garnett, G. P., Hagan, P., Hii, J. K. L., Ndhlovu, P. D., Quinnell, R. J., Watts, C. H., Chandiwana, S. K. and Anderson, R. M. (1997). Heterogeneities in the transmission of infectious agents : implications for the design of control programs. Proceedings of the National Academy of Sciences USA 94, 338342. doi: 10.1073/pnas.94.1.338.Google Scholar
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