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Effects of the social environment on the survival and fungal resistance of ant brood

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Abstract

The phenotype of social animals can be influenced by genetic, maternal and environmental effects, which include social interactions during development. In social insects, the social environment and genetic origin of brood can each influence a whole suite of traits, from individual size to caste differentiation. Here, we investigate to which degree the social environment during development affects the survival and fungal resistance of ant brood of known maternal origin. We manipulated one component of the social environment, the worker/brood ratio, of brood originating from single queens of Formica selysi. We monitored the survival of brood and measured the head size and ability to resist the entomopathogenic fungus Beauveria bassiana of the resulting callow workers. The worker/brood ratio and origin of eggs affected the survival and maturation time of the brood and the size of the resulting callow workers. The survival of the callow workers varied greatly according to their origin, both in controls and when challenged with B. bassiana. However, there was no interaction between the fungal challenge and either the worker/brood ratio or origin of eggs, suggesting that these factors did not affect parasite resistance in the conditions tested. Overall, the social conditions during brood rearing and the origin of eggs had a strong impact on brood traits that are important for fitness. We detected a surprisingly large amount of variation among queens in the survival of their brood reared in standard queenless conditions, which calls for further studies on genetic, maternal and social effects influencing brood development in the social insects.

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References

  • Abril S, Oliveras J, Crisanto G (2010) Effect of temperature on the development and survival of the Argentine ant, Linepithema humile. J Insect Sci 10:1–13

    Article  Google Scholar 

  • Billick I (2001) Density dependence and colony growth in the ant species Formica neorufibarbis. J Anim Ecol 70:895–905

    Article  Google Scholar 

  • Billick I, Carter C (2007) Testing the importance of the distribution of worker sizes to colony performance in the ant species Formica obscuripes Forel. Insect Soc 54:113–117

    Article  Google Scholar 

  • Brian MV (1953) Brood-rearing in relation to worker number in the ant Myrmica. Physiol Zool 26:355–366

    Google Scholar 

  • Brian MV (1957) The growth and development of colonies of the ant Myrmica. Insect Soc 4:177–190

    Article  Google Scholar 

  • Brian MV, Carr CAH (1960) The influence of the queen on brood rearing in ants of the genus Myrmica. J Insect Physiol 5:81–94

    Article  Google Scholar 

  • Calleri DV, Reid EM, Rosengaus RB, Vargo EL, Traniello JFA (2006) Inbreeding and disease resistance in a social insect: effects of heterozygosity on immunocompetence in the termite Zootermopsis angusticollis. Proc R Soc Lond B 273:2633–2640

    Article  Google Scholar 

  • Cassill D (2002) Brood care strategies by newly mated monogyne Solenopsis invicta (Hymenoptera: Formicidae) queens during colony founding. Ann Entomol Soc Am 95:208–212

    Article  Google Scholar 

  • Cassill DL, Tschinkel WR (1999) Effects of colony-level attributes on larval feeding in the fire ant, Solenopsis invicta. Insect Soc 46:261–266

    Article  Google Scholar 

  • Castella G, Christe P, Chapuisat M (2010) Covariation between colony social structure and immune defences of workers in the ant Formica selysi. Insect Soc 57:233–238

    Article  Google Scholar 

  • Castilho AMC, Fraga ME, Aguiar-Menezes EL, Rosa CAR (2010) Selection of Metarhizium anisopliae and Beauveria bassiana isolates pathogenic to Atta bisphaerica and Atta sexdens rubropilosa soldiers under laboratory conditions. Cienc Rural 40:1243–1249

    Article  Google Scholar 

  • Chapuisat M, Bocherens S, Rosset H (2004) Variable queen number in ant colonies: no impact on queen turnover, inbreeding, and population genetic differentiation in the ant Formica selysi. Evolution 58:1064–1072

    PubMed  Google Scholar 

  • Chapuisat M, Oppliger A, Magliano P, Christe P (2007) Wood ants use resin to protect themselves against pathogens. Proc R Soc Lond B 274:2013–2017

    Article  Google Scholar 

  • Cotter SC, Kruuk LEB, Wilson K (2004) Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. J Evol Biol 17:421–429

    Article  PubMed  CAS  Google Scholar 

  • Cremer S, Armitage SAO, Schmid-Hempel P (2007) Social immunity. Curr Biol 17:R693–R702

    Article  PubMed  CAS  Google Scholar 

  • Evesham EJM (1985) The interaction of food distribution and the caste composition of an ant colony (Myrmica rubra L.). J Zool 207:241–250

    Article  Google Scholar 

  • Fournier D, Battaille G, Timmermans I, Aron S (2008) Genetic diversity, worker size polymorphism and division of labour in the polyandrous ant Cataglyphis cursor. Anim Behav 75:151–158

    Article  Google Scholar 

  • Gray B (1971) A morphometric study of the ant species, Myrmecia dispar (Clark). Insect Soc 18:95–110

    Article  Google Scholar 

  • Hamilton C, Lejeune BT, Rosengaus RB (2011) Trophallaxis and prophylaxis: social immunity in the carpenter ant Camponotus pennsylvanicus. Biol Lett 7:89–92

    Article  PubMed  Google Scholar 

  • Hartmann A, Wantia J, Torres JA, Heinze J (2003) Worker policing without genetic conflicts in a clonal ant. Proc Natl Acad Sci USA 100:12836–12840

    Article  PubMed  CAS  Google Scholar 

  • Heinze J (2008) Social plasticity: ecology, genetics, and the structure of ant societies. In: Korb J, Heinze J (eds) Ecology of social evolution. Springer-Verlag, Berlin, pp 129–150

    Chapter  Google Scholar 

  • Holzer B, Kümmerli R, Keller L, Chapuisat M (2006) Sham nepotism as a result of intrinsic differences in brood viability in ants. Proc R Soc Lond B 273:2049–2052

    Article  Google Scholar 

  • Howard KJ, Jeanne RL (2004) Rates of brood development in a social wasp: effects of colony size and parasite infection. Insect Soc 51:179–185

    Article  Google Scholar 

  • Hughes WOH, Boomsma JJ (2004) Genetic diversity and disease resistance in leaf-cutting ant societies. Evolution 58:1251–1260

    PubMed  Google Scholar 

  • Kapheim KM, Bernal SP, Smith AR, Nonacs R, Wcislo WT (2011) Support for maternal manipulation of developmental nutrition in a facultatively eusocial bee, Megaloptis genalis (Halictidae). Behav Ecol Sociobiol 65:1179–1190

    Article  PubMed  Google Scholar 

  • Keller L (1988) Evolutionary implications of polygyny in the Argentine ant, Iridomyrmex humilis (Mayr) (Hymenoptera: Formicidae): an experimental study. Anim Behav 36:159–165

    Article  Google Scholar 

  • Keller L, Reeve HK (1994) Partitioning of reproduction in animal societies. Trends Ecol Evol 9:98–102

    Article  PubMed  CAS  Google Scholar 

  • Kovacs JL, Hoffman EA, Marriner SM, Rekau JA, Goodisman MAD (2010) Environmental and genetic influences on queen and worker body size in the social wasp Vespula maculifrons. Insect Soc 57:53–65

    Article  Google Scholar 

  • Linksvayer TA (2006) Direct, maternal, and sibsocial genetic effects on individual and colony traits in an ant. Evolution 60:2552–2561

    PubMed  Google Scholar 

  • Linksvayer TA (2007) Ant species differences determined by epistasis between brood and worker genomes. PLoS One 2(10):e994

    Article  PubMed  Google Scholar 

  • Linksvayer TA (2008) Queen-worker-brood coadaptation rather than conflict may drive colony resource allocation in the ant Temnothorax curvispinosus. Behav Ecol Sociobiol 62:647–657

    Article  Google Scholar 

  • Linksvayer TA, Wade MJ (2005) The evolutionary origin and elaboration of sociality in the aculeate Hymenoptera: maternal effects, sib-social effects, and heterochrony. Q Rev Biol 80:317–336

    Article  PubMed  Google Scholar 

  • Lubach GR, Coe CL, Ershler WB (1995) Effects of early rearing environment on immune-responses of infant Rhesus monkeys. Brain Behav Immun 9:31–46

    Article  PubMed  CAS  Google Scholar 

  • Meaney MJ (2001) Nature, nurture, and the disunity of knowledge. Ann NY Acad Sci 935:50–61

    Article  PubMed  CAS  Google Scholar 

  • Meunier J, Chapuisat M (2009) The determinants of queen size in a socially polymorphic ant. J Evol Biol 22:1906–1913

    Article  PubMed  CAS  Google Scholar 

  • Moreno-Garcia M, Lanz-Mendoza H, Cordoba-Aguilar A (2010) Genetic variance and genotype-by-environment interaction of immune response in Aedes aegypti (Diptera: Culicidae). J Med Entomol 47:111–120

    Article  PubMed  CAS  Google Scholar 

  • Mukawa S, Tooyama H, Ikegami T (2011) Influence of humidity on the infection of western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae), by Beauverian bassiana. Appl Entomol Zool 46:255–264

    Article  Google Scholar 

  • Porter SD, Tschinkel WR (1985) Fire ant polymorphism (Hymenoptera: Formicidae): factors affecting worker size. Ann Entomol Soc Am 78:381–386

    Google Scholar 

  • Prager G, Stefanski V, Hudson R, Roedel HG (2010) Family matters: maternal and litter-size effects on immune parameters in young laboratory rats. Brain Behav Immun 24:1371–1378

    Article  PubMed  CAS  Google Scholar 

  • Reber A, Chapuisat M (in press) Diversity, prevalence and virulence of fungal entomopathogens in colonies of the ant Formica selysi. Insect Soc

  • Reber A, Castella G, Christe P, Chapuisat M (2008) Experimentally increased group diversity improves disease resistance in an ant species. Ecol Lett 11:682–689

    Article  PubMed  Google Scholar 

  • Reber A, Purcell J, Buechel SD, Buri R, Chapuisat M (2011) The expression and impact of antifungal grooming in ants. J Evol Biol 24:954–964

    Article  PubMed  CAS  Google Scholar 

  • Rosset H, Chapuisat M (2007) Alternative life-histories in a socially polymorphic ant. Evol Ecol 21:577–588

    Article  Google Scholar 

  • Russell AF, Lummaa V (2009) Maternal effects in cooperative breeders: from hymenopterans to humans. Philos T R Soc Lond B 364:1143–1167

    Article  Google Scholar 

  • Saino N, Calza S, Møller AP (1997) Immunocompetence of nestling barn swallows in relation to brood size and parental effort. J Anim Ecol 66:827–836

    Article  Google Scholar 

  • Schwander T, Rosset H, Chapuisat M (2005) Division of labour and worker size polymorphism in ant colonies: the impact of social and genetic factors. Behav Ecol Sociobiol 59:215–221

    Article  Google Scholar 

  • Schwander T, Lo N, Beekman M, Oldroyd BP, Keller L (2010) Nature versus nurture in social insect caste differentiation. Trends Ecol Evol 25:275–282

    Article  PubMed  Google Scholar 

  • Soler JJ, Moreno J, Potti J (2003) Environmental, genetic and maternal components of immunocompetence of nestling pied flycatchers from a cross-fostering study. Evol Ecol Res 5:259–272

    Google Scholar 

  • Suwanchaichinda C, Paskewitz SM (1998) Effects of larval nutrition, adult body size, and adult temperature on the ability of Anopheles gambiae (Diptera: Culicidae) to melanize sephadex beads. J Med Entomol 35:157–161

    PubMed  CAS  Google Scholar 

  • Tschinkel WR (1988) Colony growth and the ontogeny of worker polymorphism in the fire ant, Solenopsis invicta. Behav Ecol Sociobiol 22:103–115

    Article  Google Scholar 

  • Valtonen TM, Roff DA, Rantala MJ (2011) Analysis of the effects of early nutritional environment on inbreeding depression in Drosophila melanogaster. J Evol Biol 24:196–205

    Article  PubMed  CAS  Google Scholar 

  • Vienne C, Errard C, Lenoir A (1998) Influence of the queen on worker behaviour and queen recognition behaviour in ants. Ethology 104:431–446

    Article  Google Scholar 

  • Vitikainen E, Sundström L (2011) Inbreeding and caste-specific variation in immune defence in the ant Formica exsecta. Behav Ecol Sociobiol 65:899–907

    Article  Google Scholar 

  • Wilson EO (1983) Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta): IV. Colony ontogeny of A. cephalotes. Behav Ecol Sociobiol 14:55–60

    Article  Google Scholar 

  • Wolf JB, Brodie ED III, Cheverud JM, Moore AJ, Wade MJ (1998) Evolutionary consequences of indirect genetic effects. Trends Ecol Evol 13:64–69

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Alain Reymond and Dominique Bays for their help with data collection. Thanks also extended to Alan Brelsford and three anonymous reviewers for comments on the manuscript. This study was funded by a Swiss National Science Foundation grant (31003A_125306) to MC.

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Correspondence to Jessica Purcell.

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Communicated by J. Heinze

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Purcell, J., Brütsch, T. & Chapuisat, M. Effects of the social environment on the survival and fungal resistance of ant brood. Behav Ecol Sociobiol 66, 467–474 (2012). https://doi.org/10.1007/s00265-011-1293-0

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  • DOI: https://doi.org/10.1007/s00265-011-1293-0

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