Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE

Worker heterozygosity and immune response in feral and managed honeybees (Apis mellifera)

E. C. Lowe A , L. W. Simmons A and B. Baer A B C
+ Author Affiliations
- Author Affiliations

A Centre for Evolutionary Biology, School of Animal Biology (M092), The University of Western Australia, Crawley, WA 6009, Australia.

B ARC Centre of Excellence in Plant Energy Biology, Bayliss Building, The University of Western Australia, Crawley, WA 6009, Australia.

C Corresponding author. Email: boris.baer@uwa.edu.au

Australian Journal of Zoology 59(2) 73-78 https://doi.org/10.1071/ZO11041
Submitted: 21 June 2011  Accepted: 5 September 2011   Published: 7 October 2011

Abstract

Genetic diversity in workers influences colony immunity in several species of eusocial insects. Much less work has been conducted to test for comparable effects of worker heterozygosity, a measure of genetic diversity within an individual. Here we present a field study using the honeybee (Apis mellifera) and sampled foraging workers throughout Western Australia. Samples were taken from feral and managed colonies, aiming to maximise the variation in worker and colony heterozygosity. We quantified worker heterozygosity using microsatellites, and tested the idea that individual worker heterozygosity predicts immune response, measured as the enzymatic activity of an antimicrobial peptide phenoloxidase (PO) and encapsulation response. We found substantial variation in worker heterozygosity, but no significant effects of heterozygosity on PO activity or encapsulation response, either on the individual or colony level. Heterozygosity was found to be higher in workers of feral colonies compared with managed colonies. Colonies kept in husbandry, as compared with colonies from the field, had significantly higher levels of PO activity and encapsulation response, providing evidence for substantial environmental effects on individual and colony immunity.

Additional keywords: encapsulation response, genetic diversity, immunity, phenoloxidase activity.


References

Armitage, S., Boomsma, J. J., and Baer, B. (2010). Diploid male production in a leaf-cutting ant. Ecological Entomology 35, 175–182.
Diploid male production in a leaf-cutting ant.CrossRef |

Baer, B., and Schmid-Hempel, P. (1999). Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 397, 151–154.
Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee.CrossRef | 1:CAS:528:DyaK1MXntVyhtQ%3D%3D&md5=ab4bee8ad239a6fc4822217e4599ec2aCAS |

Baer, B., and Schmid-Hempel, P. (2001). Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, Bombus terrestris. Evolution 55, 1639–1643.
| 1:STN:280:DC%2BD3Mrjtlartw%3D%3D&md5=f6deaee2b259ad6f060a54252ac83172CAS |

Baer, B., and Schmid-Hempel, P. (2005). Sperm influences female hibernation success, survival and fitness in the bumblebee Bombus terrestris. Proceedings. Biological Sciences 272, 319–323.
Sperm influences female hibernation success, survival and fitness in the bumblebee Bombus terrestris.CrossRef |

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, 298–303.
Examination of the immune responses of males and workers of the leaf-cutting ant Acromyrmex echinatior and the effect of infection.CrossRef |

Baer, B., Armitage, S. A. O., and Boomsma, J. J. (2006). Sperm storage induces an immunity cost in ants. Nature 441, 872–875.
Sperm storage induces an immunity cost in ants.CrossRef | 1:CAS:528:DC%2BD28XlvVGlsbk%3D&md5=cd488b7c9b545b4ae02924a9e68a8119CAS |

Bensch, S., Andrén, H., Hansson, B., Pedersen, H. C., Sand, H., Sejberg, D., Wabakken, P., Åkesson, M., and Liberg, O. (2006). Selection for heterozygosity gives hope to a wild population of inbred wolves. PLoS ONE 1, e72.
Selection for heterozygosity gives hope to a wild population of inbred wolves.CrossRef |

Bonneaud, C., Mazuc, J. R. M., Gonzalez, G., Haussy, C., Chastel, O., Faivre, B., and Sorci, G. (2003). Assessing the cost of mounting an immune response. American Naturalist 161, 367–379.
Assessing the cost of mounting an immune response.CrossRef |

Boomsma, J. J., and Ratnieks, F. L. W. (1996). Paternity in eusocial Hymenoptera. Philosophical Transactions of the Royal Society B 351, 947–975.
Paternity in eusocial Hymenoptera.CrossRef |

Boomsma, J. J., Baer, B., and Heinze, J. (2005). The evolution of male traits in social insects. Annual Review of Entomology 50, 395–420.
The evolution of male traits in social insects.CrossRef | 1:CAS:528:DC%2BD2MXhtFOqtLk%3D&md5=4f79b3ca0623ab2ebef4e737682f7b49CAS |

Borrell, Y. J., Pineda, H., McCarthy, I., Vazquez, E., Sanchez, J. A., and Lizana, G. B. (2004). Correlations between fitness and heterozygosity at allozyme and microsatellite loci in the Atlantic salmon, Salmo salar L. Heredity 92, 585–593.
Correlations between fitness and heterozygosity at allozyme and microsatellite loci in the Atlantic salmon, Salmo salar L.CrossRef | 1:CAS:528:DC%2BD2cXkt1Ggtrc%3D&md5=af58b24eb34fd1f1dc6faa0221fb9e9cCAS |

Britten, H. B. (1996). Meta-analyses of the association between multilocus heterozygosity and fitness. Evolution 50, 2158–2164.
Meta-analyses of the association between multilocus heterozygosity and fitness.CrossRef |

Brown, J. L. (1997). A theory of mate choice based on heterozygosity. Behavioral Ecology 8, 60–65.
A theory of mate choice based on heterozygosity.CrossRef |

Chapman, J. R., Nakagawa, S., Coltman, D. W., Slate, J., and Sheldon, B. C. (2009). A quantitative review of heterozygosity fitness correlations in animal populations. Molecular Ecology 18, 2746–2765.
A quantitative review of heterozygosity fitness correlations in animal populations.CrossRef | 1:CAS:528:DC%2BD1MXpvFeiurg%3D&md5=6b7425802d7e618be245ad3fb24d3244CAS |

Chapman, N. C., Lim, J., and Oldroyd, B. P. (2008). Population genetics of commercial and feral honey bees in Western Australia. Journal of Economic Entomology 101, 272–277.
Population genetics of commercial and feral honey bees in Western Australia.CrossRef | 1:CAS:528:DC%2BD1cXltlOisro%3D&md5=fbd91aa6a2a47b79d0ef78b82595a295CAS |

Crozier, R. H., and Fjerdingstad, E. J. (2001). Polyandy in social hymenoptera: disunity in diversity. Annales Zoologici Fennici 38, 267–285.

DeWoody, Y. D., and DeWoody, J. A. (2004). On the estimation of genome-wide heterozygosity using molecular markers. The Journal of Heredity 96, 85–88.
On the estimation of genome-wide heterozygosity using molecular markers.CrossRef |

Doums, C., and Schmid-Hempel, P. (2000). Immunocompetence in workers of a social insect, Bombus terrestris L., in relation to foraging activity and parasitic infection. Canadian Journal of Zoology 78, 1060–1066.

Estoup, A., Garnery, L., Solignac, M., and Cornuet, J. M. (1995). Microsatellite variation in honey bee (Apis mellifera L.) populations: hierarchical genetic structure and test of the infinite allele and stepwise mutation models. Genetics 140, 679–695.
| 1:CAS:528:DyaK28Xht1CgsL8%3D&md5=4a50f74bdec648006a7277674e567f2aCAS |

Evans, J. D., and Pettis, J. S. (2005). Colony-level impacts of immune responsiveness in honey bees, Apis mellifera. Evolution 59, 2270–2274.
| 1:CAS:528:DC%2BD2MXht1ClsrbN&md5=efc7f75410d47701f26cc5433b901b2cCAS |

Fewell, J. H., and Gadau, J. (2009). ‘Organization of Insect Societies: From Genome to Social Complexity.’ (Harvard University Press: Cambridge, MA.)

Fossøy, F., Johnsen, A., and Lifjeld, J. T. (2009). Cell-mediated immunity and multi-locus heterozygosity in bluethroat nestlings. Journal of Evolutionary Biology 22, 1954–1960.
Cell-mediated immunity and multi-locus heterozygosity in bluethroat nestlings.CrossRef |

Franck, P., Garnery, L., Loiseau, A., Oldroyd, B. P., Hepburn, H. R., Solignac, M., and Cornuet, J. M. (2001). Genetic diversity of the honeybee in Africa: microsatellite and mitochondrial data. Heredity 86, 420–430.
Genetic diversity of the honeybee in Africa: microsatellite and mitochondrial data.CrossRef | 1:CAS:528:DC%2BD3MXmsVyjsLo%3D&md5=53b077171b6117092c856b0ac37b9171CAS |

Gerloff, C. U., Ottmer, B. K., and Schmid-Hempel, P. (2003). Effects of inbreeding on immune response and body size in a social insect, Bombus terrestris. Functional Ecology 17, 582–589.
Effects of inbreeding on immune response and body size in a social insect, Bombus terrestris.CrossRef |

Hamilton, W. D. (1964). The genetical evolution of social behaviour. Journal of Theoretical Biology 7, 1–16.
The genetical evolution of social behaviour.CrossRef | 1:STN:280:DyaF2s7jtVehsA%3D%3D&md5=d80171da5c52dfa1fef0aaa6ec1cec9dCAS |

Hansson, B., and Westerberg, L. (2002). On the correlation between heterozygosity and fitness in natural populations. Molecular Ecology 11, 2467–2474.
On the correlation between heterozygosity and fitness in natural populations.CrossRef |

Hawley, D. M., Sydenstricker, K. V., Kollias, G. V., and Dhondt, A. A. (2005). Genetic diversity predicts pathogen resistance and cell-mediated immunocompetence in house finches. Biology Letters 1, 326–329.
Genetic diversity predicts pathogen resistance and cell-mediated immunocompetence in house finches.CrossRef |

Hillyer, J. F., and Christensen, B. M. (2005). Mosquito phenoloxidase and defensin colocalize in melanization innate immune responses. The Journal of Histochemistry and Cytochemistry 53, 689–698.
Mosquito phenoloxidase and defensin colocalize in melanization innate immune responses.CrossRef | 1:CAS:528:DC%2BD2MXkvF2lu7Y%3D&md5=2582e3393e278a16676921d9c95fa22bCAS |

Hughes, W. O. H., Oldroyd, B. P., Beekman, M., and Ratnieks, F. L. W. (2008). Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320, 1213–1216.
Ancestral monogamy shows kin selection is key to the evolution of eusociality.CrossRef | 1:CAS:528:DC%2BD1cXmt1Oisrs%3D&md5=1bbfd2002cbe177ebf2d084fb74e8aa1CAS |

Jaffé, R., Moritz, R. F. A., and Kraus, F. B. (2009). Gene flow is maintained by polyandry and male dispersal in the army ant Eciton burchellii. Population Ecology 51, 227–236.
Gene flow is maintained by polyandry and male dispersal in the army ant Eciton burchellii.CrossRef |

Keller, L., and Reeve, H. K. (1994). Genetic variability, queen number, and polyandry in social hymenoptera. Evolution 48, 694–704.
Genetic variability, queen number, and polyandry in social hymenoptera.CrossRef |

Lambrechts, L., Vulule, J. M., and Koella, J. C. (2004). Genetic correlation between melanization and antibacterial immune responses in a natural population of the malaria vector Anopheles gambiae. Evolution 58, 2377–2381.

Liu, H., Jiravanichpaisal, P., Cerenius, L., Lee, B. L., Sorderhall, I., and Soderhall, K. (2007). Phenoloxidase is an important component of the defense against Aeromonas hydrophila infection in a crustacean, Pacifastacus leniusculus. The Journal of Biological Chemistry 282, 33593–33598.
Phenoloxidase is an important component of the defense against Aeromonas hydrophila infection in a crustacean, Pacifastacus leniusculus.CrossRef | 1:CAS:528:DC%2BD2sXht1Oqsr%2FL&md5=71f1eb418daa65e6fe16017c7446d4eeCAS |

Lochmiller, R. L., and Deerenberg, C. (2000). Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 87–98.
Trade-offs in evolutionary immunology: just what is the cost of immunity?CrossRef |

Mattila, H. R., and Seeley, T. D. (2007). Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317, 362–364.
Genetic diversity in honey bee colonies enhances productivity and fitness.CrossRef | 1:CAS:528:DC%2BD2sXnslGrs74%3D&md5=889524d9df4847ef86abce4707daeb1cCAS |

Meznar, E. R., Gadau, J., Koeniger, N., and Rueppell, O. (2010). Comparative linkage mapping suggests a high recombination rate in all honeybees. The Journal of Heredity 101, 118–126.
Comparative linkage mapping suggests a high recombination rate in all honeybees.CrossRef |

Oldroyd, B. P., and Fewell, J. H. (2007). Genetic diversity promotes homeostasis in insect colonies. Trends in Ecology & Evolution 22, 408–413.
Genetic diversity promotes homeostasis in insect colonies.CrossRef |

Oldroyd, B. P., and Thompson, G. J. (2006). Behavioural genetics of the honey bee, Apis mellifera. Advances in Insect Physiology 33, 1–49.
Behavioural genetics of the honey bee, Apis mellifera.CrossRef |

Pogson, G. H., and Fevolden, S. E. (1998). DNA heterozygosity and growth rate in the Atlantic cod Gadus morhua (L). Evolution 52, 915–920.
DNA heterozygosity and growth rate in the Atlantic cod Gadus morhua (L).CrossRef |

Ratcliffe, N. A., Leonard, C., and Rowley, A. F. (1984). Prophenoloxidase activation: nonself recognition and cell cooperation in insect immunity. Science 226, 557–559.
Prophenoloxidase activation: nonself recognition and cell cooperation in insect immunity.CrossRef | 1:CAS:528:DyaL2cXmt1ynsrc%3D&md5=bb500bb0ca7d1c407f81f3b40633f961CAS |

Rousset, F. (2008). Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources 8, 103–106.
Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux.CrossRef |

Rowe, G., Beebee, T. J. C., and Burke, T. (1999). Microsatellite heterozygosity, fitness and demography in natterjack toads Bufo calamita. Animal Conservation 2, 85–92.
Microsatellite heterozygosity, fitness and demography in natterjack toads Bufo calamita.CrossRef |

Schmid, M. R., Brockmann, A., Pirk, C. W. W., Stanley, D. W., and Tautz, J. (2008). Adult honeybees (Apis mellifera L.) abandon hemocytic, but not phenoloxidase immunity. Journal of Insect Physiology 54, 439–444.
Adult honeybees (Apis mellifera L.) abandon hemocytic, but not phenoloxidase immunity.CrossRef | 1:CAS:528:DC%2BD1cXhsVSnurc%3D&md5=b56c1521af8684abd629199b92b4e29eCAS |

Schmid-Hempel, P. (1998). ‘Parasites in Social Insects.’ Monographs in Behavior and Ecology. (Princeton University Press, Princeton, NJ.)

Seddon, N., Amos, W., Mulder, R. A., and Tobias, J. A. (2004). Male heterozygosity predicts territory size, song structure and reproductive success in a cooperatively breeding bird. Proceedings of the Royal Society of London. Series B. Biological Sciences 271, 1823–1829.
Male heterozygosity predicts territory size, song structure and reproductive success in a cooperatively breeding bird.CrossRef |

Sherman, P. W., Seeley, T. D., and Hudson, K. R. (1988). Parasites, pathogens, and polyandry in social Hymenoptera. American Naturalist 131, 602–610.
Parasites, pathogens, and polyandry in social Hymenoptera.CrossRef |

Simmons, L. W., Zuk, M., and Rotenberry, J. T. (2005). Immune function reflected in calling song characteristics in a natural population of the cricket Teleogryllus commodus. Animal Behaviour 69, 1235–1241.
Immune function reflected in calling song characteristics in a natural population of the cricket Teleogryllus commodus.CrossRef |

Simmons, L. W., Beveridge, M., Wedell, N., and Tregenza, T. (2006). Post-copulatory inbreeding avoidance by female crickets only revealed by molecular markers. Molecular Ecology 15, 3817–3824.
Post-copulatory inbreeding avoidance by female crickets only revealed by molecular markers.CrossRef | 1:CAS:528:DC%2BD28Xht1OisLrM&md5=47b350de484556ede88b6925f5ef1ca8CAS |

Sirvio, A., Gadau, J., Rueppell, O., Lamatsch, D., Boomsma, J. J., Pamilo, P., and Page, R. E. (2006). High recombination frequency creates genotypic diversity in colonies of the leaf-cutting ant Acromyrmex echinatior. Journal of Evolutionary Biology 19, 1475–1485.
High recombination frequency creates genotypic diversity in colonies of the leaf-cutting ant Acromyrmex echinatior.CrossRef | 1:STN:280:DC%2BD28vosl2gtg%3D%3D&md5=3f79ac85bdd836ad114602cff10c2cf7CAS |

Solignac, M., Vautrin, D., Loiseau, A., Mougel, F., Baudry, E., Estoup, A., Garnery, L., Michael, H., and Cornuet, J. M. (2003). Five hundred and fifty microsatellite markers for the study of the honeybee (Apis mellifera L.) genome. Molecular Ecology Notes 3, 307–311.
Five hundred and fifty microsatellite markers for the study of the honeybee (Apis mellifera L.) genome.CrossRef | 1:CAS:528:DC%2BD3sXlt12htLs%3D&md5=723ebf39ba1df08d54bd6ec5970a38aaCAS |

Strassmann, J. (2001). The rarity of multiple mating by females in the social Hymenoptera. Insectes Sociaux 48, 1–13.
The rarity of multiple mating by females in the social Hymenoptera.CrossRef |

Tarpy, D. R. (2003). Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proceedings. Biological Sciences 270, 99–103.
Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth.CrossRef |

Tarpy, D. R., and Page, R. E. (2001). The curious promiscuity of queen honey bees (Apis mellifera): evolutionary and behavioural mechanisms. Annales Zoologici Fennici 38, 255–265.

Trivers, R. L., and Hare, H. (1976). Haplodiploidy and the evolution of the social insects. Science 191, 249–263.
Haplodiploidy and the evolution of the social insects.CrossRef | 1:STN:280:DyaE287gsVGrsA%3D%3D&md5=2442b04521cb51325d76fb50a96d2903CAS |

Van Dongen, S., Backeljau, T., Matthysen, E., and Dhondt, A. A. (2007). Fitness–heterozygosity associations differ between male and female winter moths Operophtera brumata L. Belgian Journal of Zoology 137, 41–46.

Wiernasz, D. C., Hines, J., Parker, D. G., and Cole, B. J. (2008). Mating for variety increases foraging activity in the harvester ant, Pogonomyrmex occidentalis. Molecular Ecology 17, 1137–1144.
Mating for variety increases foraging activity in the harvester ant, Pogonomyrmex occidentalis.CrossRef |

Wilfert, L., Gadau, J., and Schmid-Hempel, P. (2007). Variation in genomic recombination rates among animal taxa and the case of social insects. Heredity 98, 189–197.
Variation in genomic recombination rates among animal taxa and the case of social insects.CrossRef | 1:CAS:528:DC%2BD2sXjsV2ju7s%3D&md5=be6d5f2d27eb0a84b2e7899f087590d7CAS |

Wilson-Rich, N., Dres, S. T., and Starks, P. T. (2008). The ontogeny of immunity: development of innate immune strength in the honey bee (Apis mellifera). Journal of Insect Physiology 54, 1392–1399.
The ontogeny of immunity: development of innate immune strength in the honey bee (Apis mellifera).CrossRef | 1:CAS:528:DC%2BD1cXhtFylsLzL&md5=d590bb39730baeaa1371d4e498a503b6CAS |

Woyke, J. (1963). What happens to diploid drone larvae in a honeybee colony? Journal of Apicultural Research 2, 73–75.



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