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Fertility Signaling and Partitioning of Reproduction in the Ant Neoponera apicalis

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Abstract

All individuals in social insect colonies benefit from being informed about the presence and fertility state of reproducers. This allows the established reproductive individuals to maintain their reproductive monopoly without the need for physical control, and the non-reproductive individuals to make appropriate reproductive choices. Here, we studied whether fertility signaling is responsible for the partitioning of reproduction in the ant Neoponera apicalis. This species forms small colonies from one single-mated queen, with workers establishing reproductive hierarchies when hopelessly queenless. Previous studies identified putative fertility signals, particularly the hydrocarbon 13-methylpentacosane (13-MeC25), and have shown that precise status discrimination based on these signals could be involved in the regulation of reproductive activities. Here, we extend these findings and reveal that all individuals, be they queens or workers, differ in their cuticular hydrocarbon profile according to fertility state. Proportions of 13-MeC25 were a strong predictor of an individual’s ovarian activity, and could, thus, advertise the established reproducer(s) in both queenright and queenless conditions. Furthermore, this compound might play a key role in the establishment of the reproductive hierarchy, since workers with low fertility at the onset of hierarchy formation already have relatively high amounts of 13-MeC25. Dyadic encounters showed that individuals with experimentally increased amounts of 13-MeC25 triggered less agonistic interactions from top rankers, in accord with them “advertising” higher status. Thus, these bioassays supported the use of 13-MeC25 by competing ants. This simple recognition system potentially allows permanent regulation of partitioning of reproduction in this species.

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References

  • Appleby MC (1983) The probability of linearity in hierarchies. Anim Behav 31:600–608

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2013) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.0-4. http://CRAN.R-project.org/package=lme4. Accessed 2 Oct 2013

  • Blacher P, Lecoutey E, Fresneau D, Nowbahari E (2010) Reproductive hierarchies and status discrimination in orphaned colonies of Pachycondyla apicalis ants. Anim Behav 79:99–105

    Article  Google Scholar 

  • Blomquist GJ (2010) Biosynthesis of cuticular hydrocarbons. In: Blomquist GJ, Bagnières A-G (eds) Insect hydrocarbons: biology, biochemistry, and chemical ecology. Cambridge University Press, Cambridge, pp 35–52

    Chapter  Google Scholar 

  • Bourke AFG (1988) Worker reproduction in the higher eusocial Hymenoptera. Q Rev Biol 63:291–311

    Article  Google Scholar 

  • Buczkowski G, Silverman J (2005) Context-dependent nestmate discrimination and the effect of action thresholds on exogenous cue recognition in the Argentine ant. Anim Behav 69:741–749

    Article  Google Scholar 

  • Cuvillier-Hot V, Lenoir A, Crewe R, Malosse C, Peeters C (2004) Fertility signalling and reproductive skew in queenless ants. Anim Behav 68:1209–1219

    Article  Google Scholar 

  • Dapporto L, Santini A, Dani FR, Turillazzi S (2007) Workers of a Polistes paper wasp detect the presence of their queen by chemical cues. Chem Senses 32:795–802

    Article  CAS  PubMed  Google Scholar 

  • de Biseau J-C, Passera L, Daloze D, Aron S (2004) Ovarian activity correlates with extreme changes in cuticular hydrocarbon profile in the highly polygynous ant, Linepithema humile. J Insect Physiol 50:585–593

    Article  PubMed  Google Scholar 

  • Delabie JHC, Mariano CSF, Mendes LF, Pompolo SG, Fresneau D (2008) Problemas apontados por estudos morfológicos, ecológicos e citogenéticos no gênero Pachycondyla na região Neotropical: o caso do complexo apicalis. In: Vilela EF, Santos IA, Schoereder JH, Neto JL, Serrão JE, Campos LAO (eds) Insetos sociais: da biologia à aplicação. Editora UVF, Viçosa, pp 197–222

    Google Scholar 

  • Dietemann V, Peeters C (2000) Queen influence on the shift from trophic to reproductive eggs laid by workers of the ponerine ant Pachycondyla apicalis. Insect Soc 47:223–228

    Article  Google Scholar 

  • Dietemann V, Peeters C, Liebig J, Thivet V, Hölldobler B (2003) Cuticular hydrocarbons mediate discrimination of reproductives and nonreproductives in the ant Myrmecia gulosa. Proc Natl Acad Sci U S A 100:10341–10346

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Endler A, Liebig J, Schmitt T, Parker JE, Jones GR, Schreier P, Hölldobler B (2004) Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect. Proc Natl Acad Sci U S A 101:2945–2950

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fresneau D (1994) Biology and social behaviour of a Neotropical ponerine ant (Pachycondyla apicalis). Dissertation, Université Paris 13

  • Getty T (2006) Sexually selected signals are not similar to sports handicaps. Trends Ecol Evol 21:83–88

    Article  PubMed  Google Scholar 

  • Grafen A (1990) Biological signals as handicaps. J Theor Biol 144:517–546

    Article  CAS  PubMed  Google Scholar 

  • Guédot C, Millar JG, Horton DR, Landolt PJ (2009) Identification of a sex attractant pheromone for male winterform pear psylla, Cacopsylla pyricola. J Chem Ecol 35:1437–1447

    Article  PubMed  Google Scholar 

  • Hammond RL, Keller L (2004) Conflict over male parentage in social insects. PLoS Biol 2:1472–1482

    Article  CAS  Google Scholar 

  • Hartfelder K (2000) Insect juvenile hormone: from “status quo” to high society. Braz J Med Biol Res 33:157–177

    Article  CAS  PubMed  Google Scholar 

  • Hartmann A, d’Ettorre P, Jones GR, Heinze J (2005) Fertility signalling–the proximate mechanism of worker policing in a clonal ant. Naturwissenschaften 92:282–286

    Article  CAS  PubMed  Google Scholar 

  • Heinze J, d’Ettorre P (2009) Honest and dishonest communication in social Hymenoptera. J Exp Biol 212:1775–1779

    Article  CAS  PubMed  Google Scholar 

  • Heinze J, Stengl B, Sledge MF (2002) Worker rank, reproductive status and cuticular hydrocarbon signature in the ant, Pachycondyla cf. inversa. Behav Ecol Sociobiol 52:59–65

    Article  Google Scholar 

  • Holman L (2012) Costs and constraints conspire to produce honest signaling: insights from an ant queen pheromone. Evolution 66:2094–2105

    Article  CAS  PubMed  Google Scholar 

  • Holman L, Jorgensen CG, Nielsen J, d’Ettorre P (2010) Identification of an ant queen pheromone regulating worker sterility. Proc R Soc Lond B Biol Sci 277:3793–3800

    Article  CAS  Google Scholar 

  • Howard RW (1993) Cuticular hydrocarbons and chemical communication. In: Stanley-Samuelson DW, Nelson DR (eds) Insect lipids, chemistry, biochemistry and biology. University of Nebraska Press, Lincoln, pp 177–226

    Google Scholar 

  • Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393

    Article  CAS  PubMed  Google Scholar 

  • Hsu Y, Earley RL, Wolf LL (2006) Modulation of aggressive behaviour by fighting experience: mechanisms and contest outcomes. Biol Rev 81:33–74

    Article  PubMed  Google Scholar 

  • Keller L, Nonacs P (1993) The role of queen pheromones in social insects: queen control or queen signal? Anim Behav 45:787–794

    Article  Google Scholar 

  • Lamba S, Kazi YC, Deshpande S, Natesh M, Bhadra A, Gadagkar R (2007) A possible novel function of dominance behaviour in queen-less colonies of the primitively eusocial wasp Ropalidia marginata. Behav Process 74:351–356

    Article  Google Scholar 

  • Liebig J (2010) Hydrocarbon profiles indicate fertility and dominance status in ant, bee, and wasp colonies. In: Blomquist GJ, Bagnières A-G (eds) Insect hydrocarbons: biology, biochemistry, and chemical ecology. University Press Cambridge, Cambridge, pp 254–281

    Chapter  Google Scholar 

  • Liebig J, Peeters C, Hölldobler B (1999) Worker policing limits the number of reproductives in a ponerine ant. Proc R Soc Lond B Biol Sci 266:1865–1870

    Article  Google Scholar 

  • Liebig J, Peeters C, Oldham NJ, Markstädter C, Hölldobler B (2000) Are variations in cuticular hydrocarbons of queens and workers a reliable signal of fertility in the ant Harpegnathos saltator? Proc Natl Acad Sci U S A 97:4124–4131

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Maynard Smith J, Harper DGC (1995) Animal signals: models and terminology. J Theor Biol 177:305–311

    Article  Google Scholar 

  • Monnin T (2006) Chemical recognition of reproductive status in social insects. Ann Zool Fenn 43:515–530

    Google Scholar 

  • Monnin T, Malosse C, Peeters C (1998) Solid-phase microextraction and cuticular hydrocarbon differences related to reproductive activity in queenless ant Dinoponera quadriceps. J Chem Ecol 24:473–490

    Article  CAS  Google Scholar 

  • Oliveira PS, Hölldobler B (1990) Dominance orders in the ponerine ant Pachycondyla apicalis (Hymenoptera, Formicidae). Behav Ecol Sociobiol 27:385–393

    Article  Google Scholar 

  • Ottoni EB (2000) EthoLog 2.2: a tool for the transcription and timing of behavior observation sessions. Behav Res Methods Instrum Comput 32:446–449

    Article  CAS  PubMed  Google Scholar 

  • Peeters C, Liebig J (2009) Fertility signaling as a general mechanism of regulating reproductive division of labor in ants. In: Gadau J, Fewell J (eds) Organization of insect societies: from genome to socio-complexity). Harvard University Press, Cambridge, pp 220–242

    Google Scholar 

  • R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. Accessed 18 June 2012

  • Ratnieks FLW, Foster KR, Wenseleers T (2006) Conflict resolution in insect societies. Annu Rev Entomol 51:581–608

    Article  CAS  PubMed  Google Scholar 

  • Reeve HK, Jeanne RL (2003) From individual control to majority rule: extending transactional models of reproductive skew in animal societies. Proc R Soc Lond B Biol Sci 270:1041–1045

    Article  Google Scholar 

  • Reyment RA (1989) Compositional data analysis. Terra Nov. 1:29–34

  • Searcy WA, Nowicki S (2005) The evolution of animal communication: reliability and deception in signaling systems. Princeton University Press, Princeton

    Google Scholar 

  • Smith AA, Hölldobler B, Liebig J (2008) Hydrocarbon signals explain the pattern of worker and egg policing in the ant Aphaenogaster cockerelli. J Chem Ecol 34:1275–1282

    Article  CAS  PubMed  Google Scholar 

  • Smith AA, Hölldober B, Liebig J (2009) Cuticular hydrocarbons reliably identify cheaters and allow enforcement of altruism in a social insect. Curr Biol 19:78–81

    Article  CAS  PubMed  Google Scholar 

  • Smith AA, Millar JG, Hanks LM, Suarez AV (2012) Experimental evidence that workers recognize reproductives through cuticular hydrocarbons in the ant Odontomachus brunneus. Behav Ecol Sociobiol 66:1267–1276

    Article  Google Scholar 

  • Számadó S (2011) The cost of honesty and the fallacy of the handicap principle. Anim Behav 81:3–10

    Article  Google Scholar 

  • Van Oystaeyen A, Oliveira RC, Holman L, van Zweden JS, Romero C, Oi CA, d’Ettorre P, Khalesi M, Billen J, Wackers F, Millar JG, Wenseleers T (2014) Conserved class of queen pheromones stops social insect workers from reproducing. Science 343:287–290

    Article  PubMed  Google Scholar 

  • Wenseleers T, Ratnieks FLW (2006) Comparative analysis of worker reproduction and policing in eusocial Hymenoptera supports relatedness theory. Am Nat 168:E163–E179

    Article  PubMed  Google Scholar 

  • Wenseleers T, Helanterä H, Hart A, Ratnieks FLW (2004) Worker reproduction and policing in insect societies: an ESS analysis. J Evol Biol 17:1035–1047

    Article  CAS  PubMed  Google Scholar 

  • Wilson EO (1971) The insect societies. Harvard University Press, Cambridge

    Google Scholar 

  • Wyatt TD (2014) Pheromones and animal behavior: chemical signals and signatures, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Yagound B, Blacher P, Fresneau D, Poteaux C, Châline N (2014) Status discrimination through fertility signalling allows ants to regulate reproductive conflicts. Anim Behav 93:25–35

    Article  Google Scholar 

  • Zahavi A (1975) Mate selection–a selection for a handicap. J Theor Biol 53:205–214

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Paul Devienne for help during ant collection and the building of our experimental setup, Philippe Cerdan for logistical support in the field, Jocelyn Millar and Isabelle Bataille for advice with the synthesis of 13-MeC25, and Margot Perez for statistical guidance. Two anonymous referees provided helpful comments on the manuscript. This study was supported by the Fundação de Amparo à Pesquisa do Estado da Bahia/Conselho Nacional de Desenvolvimento Científico e Tecnológico (PNX0011/2009 PRONEX).

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Authors and Affiliations

  1. Laboratoire d’Ethologie Expérimentale et Comparée, E.A. 4443, Université Paris 13, Sorbonne Paris Cité, 93430, Villetaneuse, France

    Boris Yagound, Rémi Gouttefarde, Chloé Leroy, Dominique Fresneau, Stéphane Chameron, Chantal Poteaux & Nicolas Châline

  2. Laboratoire de Recherche Vasculaire Translationnelle, INSERM U 1148, Université Paris 13, Sorbonne Paris Cité, 93430, Villetaneuse, France

    Rima Belibel & Christel Barbaud

  3. Department of Experimental Psychology, Institute of Psychology, University of São Paulo, São Paulo, Brazil

    Nicolas Châline

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  1. Boris Yagound
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Correspondence to Boris Yagound.

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Yagound, B., Gouttefarde, R., Leroy, C. et al. Fertility Signaling and Partitioning of Reproduction in the Ant Neoponera apicalis . J Chem Ecol 41, 557–566 (2015). https://doi.org/10.1007/s10886-015-0591-9

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