Skip to main content
SpringerLink
Log in

Dishonest Signaling in Vertebrate Eusociality

  • Long Article
  • Published:
Biological Theory Aims and scope Submit manuscript

Abstract

I propose that a dishonest signaling system can be evolutionarily stable in eusocial animal societies if the amount of dishonesty is balanced by the chance of non-reproductive workers to advance to the reproductive caste in the future. I express this trade-off in a modified form of Hamilton’s rule, where I distinguish between the real and perceived cost of an altruistic act, and between the real and perceived genetic relatedness between colony members. Furthermore, I elaborate how the vertebrate neuromodulator oxytocin could serve as an internal representation of the perceived cost of an altruistic act and of perceived relatedness. Behavioral and receptor localization data support this hypothesis. The encoding of cost and relatedness by oxytocin is likely integrated with a number of other functions related to social bonding. I conclude with a discussion of honesty in signaling, an outline of testable consequences of this hypothesis, and a comparison between vertebrate and insect eusociality.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Bourke AFG (2011) The validity and value of inclusive fitness theory. Proc R Soc B 278:3313–3320

    Article  Google Scholar 

  • Bullock TH (1984) Comparative neuroscience holds promise for quiet revolutions. Science 225:473–478

    Article  Google Scholar 

  • Charnov EL (1978) Evolution of eusocial behavior: offspring choice or parental parasitism? J Theor Biol 75:451–465

    Article  Google Scholar 

  • Clarke FM, Faulkes CG (1997) Dominance and queen succession in captive colonies of the eusocial naked mole–rat, Heterocephalus glaber. Proc R Soc Lond B 264:993–1000

    Article  Google Scholar 

  • De Dreu CKWD, Greer LL, Handgraaf MJJ et al (2010) The neuropeptide oxytocin regulates parochial altruism in intergroup conflict among humans. Science 328:1408–1411

    Article  Google Scholar 

  • De Dreu CKW, Shalvi S, Greer LL et al (2012) Oxytocin motivates non-cooperation in intergroup conflict to protect vulnerable in-group members. PLoS One 7:e46751

    Article  Google Scholar 

  • Faulkes CG, Bennett NC (2001) Family values: group dynamics and social control of reproduction in African mole-rats. Trends Ecol Evol 16(4):184–190

    Google Scholar 

  • Field T (2010) Touch for socioemotional and physical well-being: a review. Dev Rev 30:367–383

    Article  Google Scholar 

  • Foster KR, Wenseleers T, Ratnieks FLW (2006) Kin selection is the key to altruism. Trends Ecol Evol 21:57–60

    Article  Google Scholar 

  • Gadagkar R (1985) Kin recognition in social insects and other animals—A review of recent findings and a consideration of their relevance for the theory of kin selection. Proc Anim Sci 94(6):587–621

    Google Scholar 

  • Guiduglia KR, Nascimento AM, Amdam GV et al (2005) Vitellogenin regulates hormonal dynamics in the worker caste of a eusocial insect. FEBS Lett 579:4961–4965

    Article  Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behaviour. II. J Theor Biol 7:17–52

    Article  Google Scholar 

  • Hamilton WD (1971) Geometry for the selfish herd. J Theor Biol 31:295–311

    Article  Google Scholar 

  • Holmes MM, Goldman BD, Goldman SL et al (2009) Neuroendocrinology and sexual differentiation in eusocial mammals. Front Neuroendocrin 30:519–533

    Article  Google Scholar 

  • Hughes WOH, Oldroyd BP, Beekman M, Ratnieks FLW (2008) Ancestral monogamy shows kin selection is key to the evolution of eusociality. Sci 320(5880):1213–1216

    Google Scholar 

  • Jarvis JUM, Bennett NC (1993) Eusociality has evolved independently in two genera of bathyergid mole-rats—but occurs in no other subterranean mammal. Behav Ecol Sociobiol 33:253–260

    Article  Google Scholar 

  • Kalamatianos T, Faulkes CG, Oosthuizen MK et al (2010) Telencephalic binding sites for oxytocin and social organization: a comparative study of eusocial naked mole-rats and solitary cape mole-rats. J Comp Neurol 518:1792–1813

    Article  Google Scholar 

  • Keller L, Perrin N (1995) Quantifying the level of eusociality. Proc R Soc Lond B 260:311–315

    Article  Google Scholar 

  • Keverne EB, Curley JP (2004) Vasopressin, oxytocin and social behaviour. Curr Opin Neurobiol 14:777–783

    Article  Google Scholar 

  • Lee H-J, Macbeth AH, Pagani J et al (2009) Oxytocin: the great facilitator of life. Prog Neurobiol 88:127–151

    Google Scholar 

  • Maynard-Smith J, Harper D (2003) Animal signals. Oxford University Press, New York

    Google Scholar 

  • Mech LD, Boitani L (2003) Wolves: behavior, ecology, and conservation. University of Chicago Press

  • Michener CD, Brothers DJ (1974) Were workers of eusocial Hymenoptera initially altruistic or oppressed? Proc Nat Acad Sci 71(3):671–674

    Google Scholar 

  • Michod RE, Hamilton WD (1980) Coefficients of relatedness in sociobiology. Nature 288(5792):694–697

    Google Scholar 

  • Mooney SJ, Holmes MM (2013) Social condition and oxytocin neuron number in the hypothalamus of naked mole-rats (Heterocephalus glaber). Neuroscience 230:56–61

    Article  Google Scholar 

  • Moshitzky P, Fleischmann I, Chaimov N et al (1996) Sex-peptide activates juvenile hormone biosynthesis in the Drosophila melanogaster corpus allatum. Arch Insect Biochem Physiol 32:363–374

    Article  Google Scholar 

  • Nowak MA, Tarnita CE, Wilson EO (2010) The evolution of eusociality. Nature 466:1057–1062

    Article  Google Scholar 

  • O’Riain M, Jarvis JU (1997) Colony member recognition and xenophobia in the naked mole-rat. Anim Behav 53:487–498

    Article  Google Scholar 

  • Queller DC (1989) The evolution of eusociality: reproductive head starts of workers. Proc Natl Acad Sci USA 86:3224–3226

    Article  Google Scholar 

  • Ratnieks FLW, Wenseleers T (2008) Altruism in insect societies and beyond: voluntary or enforced? Trends Ecol Evol 23:45–52

    Article  Google Scholar 

  • Reeve HK (1992) Queen activation of lazy workers in colonies of the eusocial naked molerat. Nature 358(6382):147–149

    Google Scholar 

  • Robinson GE, Vargo EL (1997) Juvenile hormone in adult eusocial hymenoptera: gonadotropin and behavioral pacemaker. Arch Insect Biochem Physiol 35:559–583

    Article  Google Scholar 

  • Rosen GJ, de Vries GJ, Goldman SL et al (2008) Distribution of oxytocin in the brain of a eusocial rodent. Neuroscience 155:809–817

    Article  Google Scholar 

  • Shanas U, Terkel J (1997) Mole-rat harderian gland secretions inhibit aggression. Anim Behav 54:1255–1263

    Article  Google Scholar 

  • Smith TE, Faulkes CG, Abbott DH (1997) Combined olfactory contact with the parent colony and direct contact with nonbreeding animals does not maintain suppression of ovulation in female naked mole-rats (Heterocephalus glaber). Horm Behav 31:277–288

    Article  Google Scholar 

  • Stiefel KM (2013) Why are there no eusocial fishes? Biol Theory 7:204–210

    Article  Google Scholar 

  • Sturgis SJ, Gordon DM (2012) Nestmate recognition in ants (Hymenoptera: Formicidae): a review. Myrmecol News 16:101–110

    Google Scholar 

  • Teal PEA, Gomez-Simuta Y, Proveaux AT (2000) Mating experience and juvenile hormone enhance sexual signaling and mating in male Caribbean fruit flies. Proc Natl Acad Sci 97:3708–3712

    Article  Google Scholar 

  • Traulsen A, Nowak MA (2006) Evolution of cooperation by multilevel selection. Proc Natl Acad Sci 103:10952–10955

    Article  Google Scholar 

  • Valesky EM, Burda H, Kaufmann R et al (2012) Distribution of oxytocin- and vasopressin-immunoreactive neurons in the brain of the eusocial mole rat (Fukomys anselli). Anat Rec 295:474–480

    Article  Google Scholar 

  • Vehrencamp SL (1983) A model for the evolution of despotic versus egalitarian societies. Anim Behav 31:667–682

    Article  Google Scholar 

  • Wenseleers T (2006) Modelling social evolution: the relative merits and limitations of a Hamilton’s rule-based approach. J Evol Biol 19:1419–1422

    Article  Google Scholar 

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

    Google Scholar 

Download references

Acknowledgments

I thank Drs. Sasha Mikheyev and Walter R. Tschinkel for insightful discussions about eusociality, and Dr. André van Schaik for critically reading the manuscript.

Author information

Authors and Affiliations

  1. The MARCS Institute, University of Western Sydney, Sydney, NSW, Australia

    Klaus M. Stiefel

Authors
  1. Klaus M. Stiefel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Klaus M. Stiefel.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stiefel, K.M. Dishonest Signaling in Vertebrate Eusociality. Biol Theory 9, 325–330 (2014). https://doi.org/10.1007/s13752-014-0167-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13752-014-0167-x

Keywords

Search

Navigation