Abstract
Social organisms are constantly exposed to infectious agents via physical contact with conspecifics. While previous work has shown that disease susceptibility at the individual and group level is influenced by genetic diversity within and between group members, it remains poorly understood how group-level resistance to pathogens relates directly to individual physiology, defence behaviour and social interactions. We investigated the effects of high versus low genetic diversity on both the individual and collective disease defences in the ant Cardiocondyla obscurior. We compared the antiseptic behaviours (grooming and hygienic behaviour) of workers from genetically homogeneous and diverse colonies after exposure of their brood to the entomopathogenic fungus Metarhizium anisopliae. While workers from diverse colonies performed intensive allogrooming and quickly removed larvae covered with live fungal spores from the nest, workers from homogeneous colonies only removed sick larvae late after infection. This difference was not caused by a reduced repertoire of antiseptic behaviours or a generally decreased brood care activity in ants from homogeneous colonies. Our data instead suggest that reduced genetic diversity compromises the ability of Cardiocondyla colonies to quickly detect or react to the presence of pathogenic fungal spores before an infection is established, thereby affecting the dynamics of social immunity in the colony.
Footnotes
References
Arkush K. D., Giese A. R., Mendonca H. L., McBride A. M., Marty G. D.& Hedrick P. W. . 2002Resistance to three pathogens in the endangered winter-run chinook salmon (Oncorhynchus tshawytscha): effects of inbreeding and major histocompatibilty complex genotypes. Can. J. Fish. Aquat. Sci. 59, 966–975. (doi:10.1139/f02-066). Crossref, ISI, Google ScholarArruda W., Lübeck I., Schrank A.& Vainstein M. H. . 2005Morphological alterations of Metarhizium anisopliae during penetration of Boophilus microplus ticks. Exp. Appl. Acarol. 37, 231–244. (doi:10.1007/s10493-005-3818-6). Crossref, PubMed, ISI, Google ScholarBaer B. C.& Schmid-Hempel P. . 1999Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 397, 151–154. (doi:10.1038/16451). Crossref, ISI, Google ScholarBaer B.& Schmid-Hempel P. . 2001Unexpected consequences of polyandry for parasitism and fitness in the bumblebee Bombus terrestris. Evolution 55, 1639–1643. Crossref, PubMed, ISI, Google ScholarBaer B.& Schmid-Hempel P. . 2003Bumblebee workers from different sire groups vary in susceptibility to parasite infection. Ecol. Lett. 6, 106–110. (doi:10.1046/j.1461-0248.2003.00411.x). Crossref, ISI, Google ScholarBeshers S. N.& Fewell J. H. . 2001Models of division of labour in social insects. Annu. Rev. Entomol. 46, 413–440. (doi:10.1146/annurev.ento.46.1.413). Crossref, PubMed, ISI, Google ScholarCalleri D. V., McGrail Reid E., Rosengaus R. B., Vargo E. L.& Traniello J. F. A. . 2006Inbreeding and disease resistance in a social insect: effects of heterozygosity on immunocompetence in the termite Zootermopsis angusticollis. Proc. R. Soc. B 273, 2633–2640. (doi:10.1098/rspb.2006.3622). Link, ISI, Google ScholarCarius H. J., Little T. J.& Ebert D. . 2001Genetic variation in a host–parasite association: potential for coevolution and frequency-dependent selection. Evolution 55, 1136–1145. (doi:10.1554/0014-3820(2001)055). Crossref, PubMed, ISI, Google ScholarChriste P., Oppliger A., Bancala F., Castella G.& Chapuisat M. . 2003Evidence for collective medication in ants. Ecol. Lett. 6, 19–22. (doi:10.1046/j.1461-0248.2003.00395.x). Crossref, ISI, Google ScholarCremer S.& Heinze J. . 2003Stress grows wings: environmental induction of winged dispersal males in Cardiocondyla ants. Curr. Biol. 13, 219–223. (doi:10.1016/S0960-9822(03)00012-5). Crossref, PubMed, ISI, Google ScholarCremer S., Armitage S. A. O.& Schmid-Hempel P. . 2007Social immunity. Curr. Biol. 17, R693–R702. (doi:10.1016/j.cub.2007.06.008). Crossref, PubMed, ISI, Google ScholarCurrie C. R.& Stuart A. E. . 2001Weeding and grooming of pathogens in agriculture by ants. Proc. R. Soc. Lond. B 268, 1033–1039. (doi:10.1098/rspb.2001.1605). Link, ISI, Google ScholarGerloff C. U., Ottmer B. K.& Schmid-Hempel P. . 2003Effects of inbreeding on immune response and body size in a social insect, Bombus terrestris. Funct. Ecol. 17, 582–589. (doi:10.1046/j.1365-2435.2003.00769.x). Crossref, ISI, Google ScholarGramacho K. P.& Spivak M. . 2003Differences in olfactory sensitivity and behavioural responses among honey bees bred for hygienic behavior. Behav. Ecol. Sociobiol. 54, 472–479. (doi:10.1007/s00265-003-0643-y). Crossref, ISI, Google ScholarHaag C. R., Sakwinska O.& Ebert D. . 2003Test of synergistic interaction between infection and inbreeding in Daphnia magna. Evolution 57, 777–783. (doi:10.1111/j.0014-3820.2003.tb00289.x). Crossref, PubMed, ISI, Google ScholarHamilton W. D. . 1987Kinship, recognition, disease and intelligence. Animal societies: theories and facts (eds, Ito Y., Brown J. L.& Kikkawa J. ), pp. 81–102. Tokyo, Japan: Japan Scientific Societies Press. Google ScholarHeinze J.& Delabie J. H. C. . 2005Population structure of the male-polymorphic ant Cardiocondyla obscurior. Stud. Neotrop. Fauna E 40, 187–190. (doi:10.1080/01650520500175250). Crossref, ISI, Google ScholarHeinze J., Cremer S., Eckl N.& Schrempf A. . 2006Stealthy invaders: the biology of Cardiocondyla tramp ants. Insect. Soc. 53, 1–7. (doi:10.1007/s00040-005-0847-4). Crossref, ISI, Google ScholarHughes W. O. H.& Boomsma J. J. . 2004Genetic diversity and disease resistance in leaf-cutting ant societies. Evolution 58, 1251–1260. (doi:10.1554/03-546). Crossref, PubMed, ISI, Google ScholarHughes W. O. H., Eilenberg J.& Boomsma J. J. . 2002Trade-offs in group living: transmission and disease resistance in leaf-cutting ants. Proc. R. Soc. Lond. B 269, 1811–1819. (doi:10.1098/rspb.2002.2113). Link, ISI, Google ScholarHughes W. O. H., Bot A. N. M.& Boomsma J. J. . 2010Caste-specific expression of genetic variation in the size of antibiotic-producing glands of leaf-cutting ants. Proc. R. Soc. B 277, 609–615. (doi:10.1098/rspb.2009.1415). Link, ISI, Google ScholarJaccoud D. B., Hughes W. O. H.& Jackson C. W. . 1999The epizootiology of a Metarhizium infection in mini-nests of the leaf-cutting ant Atta sexdens rubropilosa. Entomol. Exp. Appl. 93, 51–61. (doi:10.1023/A:1003830625680). Crossref, ISI, Google ScholarKermarrec A., Febvay G.& Decharme M. . 1986Protection of leaf-cutting ants from biohazards: is there a future for microbiological control? In Fire ants and leaf-cutting ants: biology and management (eds, Lofgren C. S.& Vander Meer R. K. ), pp. 339–356. Boulder, CO: Westview Press. Google ScholarLambrechts L., Halbert J., Durand P., Gouagna L. C.& Koella J. C. . 2005Host genotype by parasite genotype interactions underlying the resistance of anopheline mosquitoes to Plasmodium falciparum. Malar. J. 4, 3. (doi:10.1186/1475-2875-4-3). Crossref, PubMed, ISI, Google ScholarLapidge K., Oldroyd B. P.& Spivak M. . 2002Seven suggestive quantitative trait loci influence hygienic behavior of honey bees. Naturwissenschaften 89, 565–568. Crossref, PubMed, ISI, Google ScholarLiersch S.& Schmid-Hempel P. . 1998Genetic variation within social insect colonies reduces parasite load. Proc. R. Soc. Lond. B 265, 221–225. (doi:10.1098/rspb.1998.0285). Link, ISI, Google ScholarLuong L. T., Heath B. D.& Polak M. . 2007Host inbreeding increases susceptibility to ectoparasitism. J. Evol. Biol. 20, 79–86. (doi:10.1111/j.1420-9101.2006.01226.x). Crossref, PubMed, ISI, Google ScholarMasterman R., Ross R., Mesce K. A.& Spivak M. . 2001Olfactory and behavioral response thresholds to odors of diseased brood differ between hygienic and nonhygienic honeybees (Apis mellifera L.). J. Comp. Physiol. 187, 441–452. Crossref, ISI, Google ScholarMattila H. R.& Seeley T. D. . 2007Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317, 362–364. (doi:10.1126/science.1143046). Crossref, PubMed, ISI, Google ScholarMburu D. M., Ochola L., Maniania N. K., Njagi P., Gitonga L., Ndungu M., Wanjoya A.& Hassanali A. . 2009Relationship between virulence and repellency of entomopathogenic isolates of Metarhizium anisopliae and Beauveria bassiana to the termite Macrotermes michaelseni. J. Insect Physiol. 55, 774–780. (doi:10.1016/j.jinsphys.2009.04.015). Crossref, PubMed, ISI, Google ScholarO'Brien S. J.& Evermann J. F. . 1988Interactive influence of infectious disease and genetic diversity in natural populations. Trends Ecol. Evol. 3, 254–259. (doi:10.1016/0169-5347(88)90058-4). Crossref, PubMed, ISI, Google ScholarOuborg N. J., Biere A.& Mudde C. L. . 2000Inbreeding effects on resistance and transmission-related traits in the Silene-Microbotryum pathosystem. Ecology 81, 520–531. ISI, Google ScholarOxley P., Spivak M.& Oldroyd B. P. . 2010Six quantitative trait loci influence task thresholds for hygienic behaviour in honeybees (Apis mellifera). Mol. Ecol. 19, 1452–1461. (doi:10.1111/j.1365-294X.2010.04569.x). Crossref, PubMed, ISI, Google ScholarPalmer K. A.& Oldroyd B. P. . 2003Evidence 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. Crossref, PubMed, ISI, Google ScholarReber A., Castella G., Christe P.& Chapuisat M. . 2008Experimentally increased group diversity improves disease resistance in an ant species. Ecol. Lett. 11, 682–689. (doi:10.1111/j.1461-0248.2008.01177.x). Crossref, PubMed, ISI, Google ScholarRosengaus R. B., Maxmen A. B., Coates L. E.& Traniello J. F. A. . 1998Disease resistance: a benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoptera: Termopsidae). Behav. Ecol. Sociobiol. 44, 125–134. (doi:10.1007/s002650050523). Crossref, ISI, Google ScholarRothenbuhler W. C.& Thompson V. C. . 1956Resistance to American foulbrood in honey bees. I. Differential survival of larvae of different genetic lines. J. Econ. Entomol. 49, 470–475. Crossref, ISI, Google ScholarSchmid-Hempel P. . 1998Parasites in social insects.Princeton, NJ: Princeton University Press. Google ScholarSchrempf A., Aron S.& Heinze J. . 2006Sex determination and inbreeding depression in an ant with regular sib-mating. Heredity 97, 75–80. (doi:10.1038/sj.hdy.6800846). Crossref, PubMed, ISI, Google ScholarSeeley T. D.& Tarpy D. R. . 2007Queen promiscuity lowers disease within honeybee colonies. Proc. R. Soc. B 274, 67–72. (doi:10.1098/rspb.2006.3702). Link, ISI, Google ScholarSherman P. W., Seeley T. D.& Reeve H. K. . 1988Parasites, pathogens, and polyandry in social Hymenoptera. Am. Nat. 131, 602–610. (doi:10.1086/284809). Crossref, ISI, Google ScholarShykoff J. A.& Schmid-Hempel P. . 1991Parasites and the advantage of genetic variability within social insect colonies. Proc. R. Soc. Lond. B 243, 55–58. (doi:10.1098/rspb.1991.0009). Link, ISI, Google ScholarSpielman D., Brook B. W., Briscoe D. A.& Frankham R. . 2004Does inbreeding and loss of genetic diversity decrease disease resistance?Conserv. Genet. 5, 439–448. (doi:10.1023/B:COGE.0000041030.76598.cd). Crossref, ISI, Google ScholarSpivak M.& Reuter G. S. . 2001Varroa destructor infestation in untreated honey bee (Hymenoptera: Apidae) colonies selected for hygienic behavior. J. Econ. Entomol. 94, 326–331. (doi:10.1603/0022-0493-94.2.326). Crossref, PubMed, ISI, Google ScholarSpivak M., Masterman R., Ross R.& Mesce K. A. . 2003Hygienic behavior in the honey bee (Apis mellifera L.) and the modulatory role of octopamine. J. Neurobiol. 55, 341–354. (doi:10.1002/neu.10219). Crossref, PubMed, Google ScholarSwanson J., Torto B., Kells S., Mesce K. A., Tumlinson J. H.& Spivak M. . 2009Odorants that induce hygienic behavior in honeybees: identification of volatile compounds in chalkbrood-infected honeybee larvae. J. Chem. Ecol. 35, 1108–1116. (doi:10.1007/s10886-009-9683-8). Crossref, PubMed, ISI, Google ScholarTarpy D. R. . 2003Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc. R. Soc. Lond. B 270, 99–103. (doi:10.1098/rspb.2002.2199). Link, ISI, Google ScholarTarpy D. R.& Seeley T. D. . 2006Lower disease infections in honeybee (Apis mellifera) colonies headed by polyandrous vs monandrous queens. Naturwissenschaften 93, 195–199. (doi:10.1007/s00114-006-0091-4). Crossref, PubMed, ISI, Google ScholarTraniello J. F. A., Rosengaus R. B.& Savoie K. . 2002The development of immunity in a social insect: evidence for the group facilitation of disease resistance. Proc. Natl Acad. Sci. USA 99, 6838–6842. (doi:10.1073/pnas.102176599). Crossref, PubMed, ISI, Google ScholarUgelvig L. V.& Cremer S. . 2007Social prophylaxis: group interaction promotes collective immunity in ant colonies. Curr. Biol. 17, 1967–1971. (doi:10.1016/j.cub.2007.10.029). Crossref, PubMed, ISI, Google ScholarVestergaard S., Butt T. M., Bresciani T. A., Gillespie A. T.& Eilenberg J. . 1999Light and electron microscopy studies of the infection of the western flower thrips Frankliniella occidentalis (Thysanoptera: Thripidae) by the entomopathogenic fungus Metarhizium anisopliae. J. Invertebr. Pathol. 73, 25–33. (doi:10.1006/jipa.1998.4802). Crossref, PubMed, ISI, Google ScholarWhiteman N. K., Matson K. D., Bollmer J. L.& Parker P. G. . 2006Disease ecology in the Galapagos Hawk (Buteo galapagoensis): host genetic diversity, parasite load and natural antibodies. Proc. R. Soc. B 273, 797–804. (doi:10.1098/rspb.2005.3396). Link, ISI, Google ScholarWilson-Rich N., Spivak M., Fefferman N. H.& Starks T. S. . 2009Genetic, individual, and group facilitation of disease resistance in insect societies. Annu. Rev. Entomol. 54, 405–423. (doi:10.1146/annurev.ento.53.103106.093301). Crossref, PubMed, ISI, Google Scholar



