Abstract
We studied the relationship between genetic diversity and disease susceptibility in honeybee colonies living under natural conditions. To do so, we created colonies in which each queen was artificially inseminated with sperm from either one or ten drones. Of the 20 colonies studied, 80% showed at least one brood disease. We found strong differences between the two types of colonies in the infection intensity of chalkbrood and in the total intensity of all brood diseases (chalkbrood, sacbrood, American foulbrood, and European foulbrood) with both variables lower for the colonies with higher genetic diversity. Our findings demonstrate that disease can be an important factor in the ecology of honeybee colonies and they provide strong support for the disease hypothesis for the evolution of polyandry by social insect queens.
This is a preview of subscription content, log in via an institution to check access.
References
Baer B, Schmid-Hempel P (1999) Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 397:151–154
Baer B, Schmid-Hempel P (2001) Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, Bombus terrestris. Evolution 55:1639–1643
Baer B, Schmid-Hempel P (2003) Bumblebee workers from different sire groups vary in susceptibility to parasite infection. Ecol Lett 6:106–110
Boomsma JJ, Fjerdingstad EJ, Frydenberg J (1999) Multiple paternity, relatedness and genetic diversity in Acromyrmex leaf-cutter ants. Proc R Soc Lond B 366:219–223
Brown MJF, Schmid-Hempel P (2003) The evolution of female multiple mating in social hymenoptera. Evolution 57:2067–2081
Crozier RH, Pamilo P (1996) Evolution of social insect colonies: sex allocation and kin selection. Oxford Univ. Press, New York
Denny AJ, Franks NR, Powell S, Edwards KJ (2004) Exceptionally high levels of multiple mating in an army ant. Naturwissenschaften 91:396–399
Haberl M, Moritz RFA (1994) Estimation of intracolonial worker relationship in a honey bee colony (Apis mellifera L.) using DNA fingerprinting. Insectes Soc 41:263–272
Hamilton WD (1987) Kinship, recognition, disease, and intelligence: constraints of social evolution. In: Ito Y, Brown JL, Kikkawa J (eds) Animal societies: theory and facts. Japanese Scientific Society, Tokyo, pp 81–102
Hughes WOH, Boomsma JJ (2004) Genetic diversity and disease resistance in leaf-cutting ant societies. Evolution 58:1251–1260
Jones JC, Myerscough MR, Graham S, Oldroyd BP (2004) Honey bee nest thermoregulation: diversity promotes stability. Science 305:402–404
Kraus B, Page RE (1998) Parasites, pathogens, and polyandry in social insects. Am Nat 151:383–391
Oldroyd BP, Rinderer TE, Buco SM (1992) Intracolonial variance in honey bee foraging behavior: the effects of sucrose concentration. J Apic Res 30:137–145
Page RE (1980) The evolution of multiple mating behavior by honey bee queens (Apis mellifera). Genetics 96:263–273
Page RE, Robinson GE, Fondrk MK, Nasr ME (1995) Effects of worker genotypic diversity on honey bee colony development and behavior (Apis mellifera L.). Behav Ecol Sociobiol 36:387–396
Palmer KA, Oldroyd BP (2003) Evidence for intra-colonial genetic variance in resistance to American foulbrood of honey bees (Apis mellifera): further support for the parasite/pathogen hypothesis for the evolution of polyandry. Naturwissenschaften 90:265–268
Ratnieks FLW (1990) The evolution of polyandry by queens in social hymenoptera: the significance of the timing of removal of diploid males. Behav Ecol Sociobiol 26:343–348
Rheindt FE, Gadau J, Strehl CP, Holldobler B (2004) Extremely high mating frequency in the Florida harvester ant (Pogonomyrmex badius). Behav Ecol Sociobiol 56:472–481
Sauter A, Brown MJF, Baer B, Schmid-Hempel P (2001) Males of social insects can prevent queens from multiple mating. Proc R Soc Lond B Biol Sci 268:1449–1454
Schmid-Hempel P (1995) Parasites and social insects. Apidologie 26:255–271
Schmid-Hempel P (1998) Parasites in Social Insects. Princeton Univ. Press, Princeton, NJ
Seeley TD (1985) Honeybee ecology: a study of adaptation in social life. Princeton Univ. Press, Princeton
Seeley TD, Visscher PK (1985) Survival of honeybees in cold climates: the critical timing of colony growth and reproduction. Ecol Entomol 10:81–88
Sherman PW, Seeley TD, Reeve HK (1988) Parasites, pathogens, and polyandry in social hymenoptera. Am Nat 131:602–610
Strassmann JE (2001) The rarity of multiple mating by females in the social hymenoptera. Insectes Soc 48:1–13
Tarpy DR (2003) Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc R Soc Lond B Biol Sci 270:99–103
Tarpy DR, Nielsen DI (2002) Sampling error, effective paternity, and estimating the genetic structure of honey bee colonies (Hymenoptera: Apidae). Ann Entomol Soc Am 95:513–528
Tarpy DR, Page RE Jr (2002) Sex determination and the evolution of polyandry in honey bees (Apis mellifera). Behav Ecol Sociobiol 52:143–150
Wiernasz DC, Perroni CL, Cole BJ (2004) Polyandry and fitness in the western harvester ant, Pogonomyrmex occidentalis. Mol Ecol 13:1601–1606
Acknowledgements
We thank Jennifer Keller, Joshua Summers, and Ben Crawley for help in the field work. This project was funded by the North Carolina Department of Agriculture & Consumer Services and by the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service, grant number 2003-35302-13387. This experiment complies with the laws of the USA.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Tarpy, D.R., Seeley, T.D. Lower disease infections in honeybee (Apis mellifera) colonies headed by polyandrous vs monandrous queens. Naturwissenschaften 93, 195–199 (2006). https://doi.org/10.1007/s00114-006-0091-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00114-006-0091-4