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Conspecific Ant Aggression is Correlated with Chemical Distance, but not with Genetic or Spatial Distance

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Abstract

Five possible mechanisms might underlie kin recognition in social groups: spatial location, familiarity through prior association, phenotype matching, recognition alleles, or rejecting unfamiliar cues. Kin recognition by phenotype matching relies on a strong correlation between genotype and phenotype. Aggression bioassays are the standard method for investigating recognition in animals, particularly social insect interactions among nestmates and non-nestmates. These bioassays typically pay little regard to how outcomes are determined by differences in chemical recognition cues of the test subjects, because the system of signal coding was unknown until recently. We exploited the known nestmate recognition system of the ant Formica exsecta to investigate aggression between 24 pairs of colonies across a range of chemical (Z9-alkene & n-alkanes), genetic, and spatial distances. The whole Z9-alkene chemical profile was the only significant (p < 0.001) predictor of aggression levels. Aggression was a nonlinear step function of Z9-alkene chemical distance, where a small change in chemical profile resulted in a rapid behavioural transition from non-aggression to overt aggression. These findings raise questions surrounding our current understanding of recognition systems, because they support phenotype matching to a colony chemical profile without a significant genetic or spatial component.

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References

  • Akino T, Yamamura K, Wakamura S, Yamaoka R (2004) Direct behavioural evidence for hydrocarbons as nest mate recognition cues in Formica japonica (Hymenoptera: Formicidae). Appl Entomol Zool 39:381–387

    Article  Google Scholar 

  • Axelrod R, Hammond RA, Grafen A (2004) Altruism via kin-selection strategies that rely on arbitrary tags with which they co-evolve. Evolution 58:1833–1838

    PubMed  Google Scholar 

  • Beecher MD, Beecher IM, Lumpkin S (1981) Parent-offspring recognition in the bank swallows (Riparia riparia): development and acoustic basis. Anim Behav 29:95–101

    Article  Google Scholar 

  • Blomquist GJ, Bagnères A-G (2010) Insect hydrocarbons; biology, biochemistry and chemical ecology. Cambridge University Press, New York, p 492

    Book  Google Scholar 

  • Boomsma JJ, Nielsen J, Sundström L, Oldham NJ, Tentschert J, Petersen HC, Morgan ED (2003) Informational constraints on optimal sex allocation in ants. Proc Nat Acad Sci 100:8799–8804

    Article  PubMed  Google Scholar 

  • Châline N, Sandoz JC, Martin SJ, Ratnieks FLW, Jones GR (2005) Learning and discrimination of individual cuticular hydrocarbons by honey bees (Apis mellifera). Chem Senses 30:327–333

    Article  PubMed  Google Scholar 

  • Chapuisat M (1996) Characterization of microsatellite loci in Formica lugubris and their variability in other ant species. Mol Ecol 5:599–601

    Article  PubMed  Google Scholar 

  • Couvillon MJ, Ratnieks FLW (2008) Odour transfer in stingless bee marmelada (Frieseomelitta varia) demonstrates that entrance guards use an “undesirable-absent” recognition system. Behav Ecol Sociobiol 62:1099–1105

    Article  Google Scholar 

  • Crozier RH (1986) Genetic clonal recognition abilities in marine invertebrates must be maintained by selection for something else. Evolution 40:1100–1101

    Article  Google Scholar 

  • Dani FR, Jones GR, Corsi S, Beard R, Pradella D, Turillazi S (2005) Nest mate recognition cues in the honey bee: differential importance of cuticular alkanes and alkenes. Chem Senses 30:1–13

    Article  Google Scholar 

  • Errard C, Hefetz A, Jaisson P (2006) Social discrimination tuning in ants: template formation and chemical similarity. Behav Ecol Sociobiol 59:353–363

    Article  Google Scholar 

  • Getz WM (1981) Genetically based kin recognition systems. J Theor Biol 92:209–226

    Article  Google Scholar 

  • Goudet J (1995) FSTAT (vers. 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). (Updated from Goudet 1995). http://www.unil.ch/izea/softwares/fstat.html. Accessed 1 March 2003

  • Greene MJ, Gordon DM (2007) Structural complexity of chemical recognition cues affects the perception of group membership in the ants Linephithema humile and Aphaenogaster cockerelli. J Exp Biol 210:897–905

    Article  PubMed  Google Scholar 

  • Guerrieri FJ, d’Ettorre P (2008) The mandible opening response: quantifying aggression elicited by chemical cues in ants. J Exp Biol 211:1109–1113

    Article  PubMed  Google Scholar 

  • Guerrieri FJ, Nehring V, Jørgensen CG, Galizia CG, D’Ettorre P (2009) Ants recognize foes and not friends. Proc Roy Soc B 276:2461–2468

    Article  Google Scholar 

  • Gyllenstrand N, Gertsch PJ, Pamilo P (2002) Polymorphic microsatellite DNA markers in the ant Formica exsecta. Mol Ecol Notes 2:67–69

    Article  Google Scholar 

  • Haag-Liautard C, Vitikainen E, Keller L, Sundström L (2009) Fitness and the level of homozygosity in a social insect. J Evol Biol 22:134–142

    Article  PubMed  Google Scholar 

  • Hasegawa E, Imai S (2004) Characterization of microsatellite loci in red wood ants Formica (s. str.) spp. and the related genus polyergus. Mol Ecol Notes 4:200–203

    Article  Google Scholar 

  • Helanterä H, Lee Y, Drijfhout FP, Martin SJ (2011) Genetic diversity, colony chemical phenotype and nestmate recognition in the ant Formica fusca. Behav Ecol 22:710–716

    Google Scholar 

  • Hölldobler B, Wilson EO (2009) The superorganism: the beauty, elegance, and strangeness of insect societies. WW Norton & Company Ltd, London

    Google Scholar 

  • Holmes WG (1984) Sibling recognition in thirteen-lined ground squirrels: effects of genetic relatedness, rearing associations, and olfaction. Behav Ecol Sociobiol 14:225–233

    Article  Google Scholar 

  • Holmes WG (2004) The early history of Hamiltonian-based research on kin recognition. Ann Zool Fennici 41:691–711

    Google Scholar 

  • Johnson BR, van Wilgenburg E, Tsutsui ND (2011) Nestmate recognition in social insects: overcoming physiological constraints with collective decision making. Behav Ecol Sociobiol 65(5):935–944 (online first)

    Article  PubMed  Google Scholar 

  • Keller L, Ross KG (1998) Selfish genes: a green beard in the red fire ant. Nature 394:573–575

    Article  Google Scholar 

  • Lacy RC, Sherman PW (1983) Kin recognition by phenotype matching. Am Nat 121:489–512

    Article  Google Scholar 

  • Martin SJ, Drijfhout FP (2009a) How reliable is the analysis of complex cuticular hydrocarbon profiles by multi-variate statistical methods? J Chem Ecol 35:375–382

    Article  PubMed  Google Scholar 

  • Martin SJ, Drijfhout FP (2009b) A review of ant cuticular hydrocarbons. J Chem Ecol 35:1151–1161

    Article  PubMed  Google Scholar 

  • Martin SJ, Helanterä H, Drijfhout FP (2008a) Colony-specific hydrocarbons identify nest mates in two species of Formica ant. J Chem Ecol 34:1072–1080

    Article  PubMed  Google Scholar 

  • Martin SJ, Vitikainen E, Helanterä H, Drijfhout FP (2008b) Chemical basis of nest mate recognition in the ant Formica exsecta. Proc Roy Soc B 275:1271–1278

    Article  Google Scholar 

  • Martin SJ, Helanterä H, Kiss K, Lee YR, Drijfhout FP (2009) Polygyny reduces rather than increases nest mate discrimination cue diversity in Formica exsecta ants. Insect Soc 56:375–383

    Article  Google Scholar 

  • Mateo JM (2009) The causal role of odours in the development of recognition templates and social preferences. Anim Behav 77:115–121

    Article  Google Scholar 

  • Morgan ED (2004) Biosynthesis in insects. Royal Society of Chemistry, Cambridge

    Google Scholar 

  • Nehring N, Evison SEF, Santorelli LA, d’Ettorre P, Hughes WO (2011) Kin-informative recognition cues in ants. Proc Roy Soc Lond B 278:1942–1948

    Article  Google Scholar 

  • Newey P (2011) Not one odour but two: a new model for nestmate recognition. J Theor Biol 270:7–12

    Article  PubMed  Google Scholar 

  • Ozaki M, Wada-Katsumata A, Fujikawa K, Iwasaki M, Yokohari F et al (2005) Ant nest mate and non-nest mate discrimination by a chemosensory sensillium. Science 309:311–315

    Article  PubMed  Google Scholar 

  • Palagi E, Dapporto L (2006) Beyond odor discrimination: demonstrating individual recognition by scent in Lemur catta. Chem Senses 31:437–443

    Article  PubMed  Google Scholar 

  • Queller DC, Goodnight KF (1997) Relatedness Version 5.0. Keck center for computation biology. Rice University, Houston

    Google Scholar 

  • Reeve HK (1989) The evolution of conspecific acceptance thresholds. Am Nat 133:407–435

    Article  Google Scholar 

  • Roulston TH, Buczkowski G, Silverman J (2003) Nestmate discrimination in ants: effect of bioassay on aggressive behaviour. Insect Soc 50:151–159

    Article  Google Scholar 

  • Rousset F, Roze D (2007) Constraints on the origin and maintenance of genetic kin recognition. Evolution 61:2320–2330

    Article  PubMed  Google Scholar 

  • Schmidt AM, d’Ettorre P, Pedersen JS (2010) Low levels of nestmate discrimination despite high genetic differentiation in the invasive pharaoh ant. Front Zool 7:20

    Article  PubMed  Google Scholar 

  • Sherman PW, Reeve HK, Pfennig DW (1997) Recognition systems. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary apporach. Blackwell Science, Oxford, pp 69–96

    Google Scholar 

  • Sundström L, Keller L, Chapuisat M (2003) Inbreeding and sex-biased gene flow in the ant Formica exsecta. Evolution 57:1552–1561

    PubMed  Google Scholar 

  • Trontti K, Tay WT, Sundström L (2003) Characterisation of polymorphic microsatellite loci for the ant Plagiolepis pygmaea. Mol Ecol Notes 3:575–577

    Article  Google Scholar 

  • Vitikainen E (2010) Causes and consequences of inbreeding in the ant Formica exsecta. Ph.D. thesis, Faculty of Biosciences, University of Helsinki, Finland

  • Wagner D, Tissot M, Gordon DM (2001) Task-related environment alters the cuticular hydrocarbon composition of harvester ants. J Chem Ecol 27:1805–1819

    Article  PubMed  Google Scholar 

  • Waldman B (1988) The ecology of kin recognition. Ann Rev Ecol Syst 19:543–571

    Article  Google Scholar 

  • Wyatt TD (2003) Pheromones and animal behaviour: communication by smell andtaste. Cambridge University Press, Cambridge

    Book  Google Scholar 

Download references

Acknowledgments

The authors thank Roger Butlin of Sheffield University for comments, and Kalle Trontti, University of Helsinki, funded by Finnish Academy grant 134561 for help in genotyping. The authors also thank Liselotte Sundström of University of Helsinki for comments and help with the Finnish field work funded by Academy of Finland grant (206505, 121216) and providing permission to work on the ant population at the Tvärminne zoological station. This study was funded by NERC grant NE/F018355/1 and NE/F018088/1.

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Authors and Affiliations

  1. Department of Animal & Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK

    Stephen J. Martin & Duncan Jackson

  2. Department of Biological and Environmental Sciences, University of Helsinki, P.O. Box 65, 00014, Helsinki, Finland

    Emma Vitikainen

  3. Chemical Ecology Group, School of Physical and Geographical Sciences, Lennard-Jones Laboratory, Keele University, Staffordshire, ST5 5BG, UK

    Falko P. Drijfhout

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  1. Stephen J. Martin
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  2. Emma Vitikainen
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  3. Falko P. Drijfhout
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  4. Duncan Jackson
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Correspondence to Stephen J. Martin.

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Edited by Bambos Kyriacou.

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Martin, S.J., Vitikainen, E., Drijfhout, F.P. et al. Conspecific Ant Aggression is Correlated with Chemical Distance, but not with Genetic or Spatial Distance. Behav Genet 42, 323–331 (2012). https://doi.org/10.1007/s10519-011-9503-0

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  • DOI: https://doi.org/10.1007/s10519-011-9503-0

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