The relative importance of spatial proximity, kin selection and potential ‘greenbeard’ signals on provisioning behaviour among helpers in a cooperative bird

Abstract

Many hypotheses have been proposed to account for cooperative behaviour, with those favouring kin selection receiving the greatest support to date. However, the importance of relatedness becomes less clear in complex societies where interactions can involve both kin and non-kin. To help clarify this, we examined the relative effect of indirect versus key direct benefit hypotheses in shaping cooperative decisions. We assessed the relative importance of likely reciprocal aid (as measured by spatial proximity between participants), kin selection (using molecular-based relatedness indices) and putative signals of relatedness (vocal similarity) on helper/helper cooperative provisioning dynamics in bell miners (Manorina melanophrys), a species living in large, complex societies. Using network analysis, we quantified the extent of shared provisioning (helping at the same nests) among individual helpers (excluding breeding pairs) over three seasons and 4290 provisioning visits, and compared these with the location of individuals within a colony and networks built using either genetic molecular relatedness or call similarity indices. Significant levels of clustering were observed in networks; individuals within a cluster were more closely related to each other than other colony members, and cluster membership was stable across years. The probability of a miner helping at another’s nest was not simply a product of spatial proximity and thus the potential for reciprocal aid. Networks constructed using helping data were significantly correlated to those built using molecular data in 5 of 10 comparisons, compared to 8 of 10 comparisons for networks constructed using call similarity. This suggests an important role of kinship in shaping helping dynamics in a complex cooperative society, apparently determined via an acoustic ‘greenbeard’ signal in this system.

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References

  1. Arnold KE, Owens IPF, Goldizen AW (2005) Division of labour within cooperatively breeding groups. Behaviour 142:1577–1590

    Article  Google Scholar 

  2. Bates D, Maechler M, Bolker BM, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. ArXiv e-print, http://arxiv.org/abs/1406.5823

  3. Bergmüller R, Johnstone RA, Russell AF, Bshary R (2007) Integrating cooperative breeding into theoretical concepts of cooperation. Behav Process 76:61–72

    Article  Google Scholar 

  4. Brown JL (1987) Helping and communal breeding in birds: ecology and evolution. Princeton University Press, Princeton, New Jersey

    Google Scholar 

  5. Browning LE, Patrick SC, Rollins LA, Griffith SC, Russell AF (2012) Kin selection, not group augmentation, predicts helping in an obligate cooperatively breeding bird. Proc R Soc Lond B 279:3861–3869

  6. Butts CT (2014) sna: tools for social network analysis. R package version 2.3-2, http://CRAN.R-project.org/package=sna

  7. Clarke MF (1989) The pattern of helping in the bell miner (Manorina melanophrys). Ethology 80:292–306

    Article  Google Scholar 

  8. Clarke MF, Fitz-Gerald GF (1994) Spatial organisation of the cooperatively breeding bell miner Manorina melanophrys. Emu 94:96–105

    Article  Google Scholar 

  9. Clarke MF, Heathcote CF (1990) Dispersal, survivorship and demography in the cooperatively breeding bell miner Manorina melanophrys. Emu 90:15–23

    Article  Google Scholar 

  10. Clauset A, Newman MEJ, Moore C (2004) Finding community structure in very large networks. Phys Rev E 70:066111

    Article  Google Scholar 

  11. Clutton-Brock TH (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296:69–72

    PubMed  CAS  Article  Google Scholar 

  12. Clutton-Brock TH (2009) Cooperation between non-kin in animal societies. Nature 462:51–57

    PubMed  CAS  Article  Google Scholar 

  13. Cockburn A (1998) Evolution of helping behavior in cooperatively breeding birds. Annu Rev Ecol Syst 29:141–177

  14. Connor RC (1986) Pseudo-reciprocity: investing in mutualism. Anim Behav 34:1562–1566

    Article  Google Scholar 

  15. Cornwallis CK, West SA, Griffin AS (2009) Routes to indirect fitness in cooperatively breeding vertebrates: kin discrimination and limited dispersal. J Evol Biol 22:2445–2457

  16. Croft DP, James R, Krause J (2008) Exploring animal social networks. Princeton University Press, Princeton, New Jersey

  17. Csardi G, Nepusz T (2006) The igraph software package for complex network research. InterJournal, Complex Systems 1695, http://igraph.org

  18. Dekker D, Krackhard D, Snijders TAB (2007) Sensitivity of MRQAP tests to collinearity and autocorellation conditions. Psychometrika 72:563–581

    PubMed  PubMed Central  Article  Google Scholar 

  19. Farine DR (2013) Animal social network inference and permutations for ecologists in R using asnipe. Meth Ecol Evol 4:1187–1194

    Article  Google Scholar 

  20. Farine DR (2014) Measuring phenotypic assortment in animal social networks: weighted associations are more robust than binary edges. Anim Behav 89:141–153

    Article  Google Scholar 

  21. Gardner A, West SA (2010) Greenbeards. Evolution 64:25–38

    PubMed  Article  Google Scholar 

  22. Godfrey SS, Ansari TH, Gardner MG, Farine DR, Bull CM (2014) A contact-based social network of lizards is defined by low genetic relatedness among strongly connected individuals. Anim Behav 97:35–43

    Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  24. Hatchwell BJ (2010) Cryptic kin selection: kin structure in vertebrate populations and opportunities for kin-directed cooperation. Ethology 116:203–216

    Article  Google Scholar 

  25. Heinsohn RG, Legge S (1999) The cost of helping. Trends Ecol Evol 14:53–57

    PubMed  Article  Google Scholar 

  26. Jetz W, Rubenstein DR (2011) Environmental uncertainty and the global biogeography of cooperative breeding in birds. Curr Biol 21:72–78

    PubMed  CAS  Article  Google Scholar 

  27. Keen SC, Meliza CD, Rubenstein DR (2013) Flight calls signal group and individual identity but not kinship in a cooperatively breeding bird. Behav Ecol 24:1279–1285

    PubMed  PubMed Central  Article  Google Scholar 

  28. Khanna H, Gaunt SLL, McCallum DA (1997) Digital spectrographic cross­correlation: tests of sensitivity. Bioacoustics 7:209–234

  29. Kokko H, Johnstone RA, Clutton-Brock TH (2001) The evolution of cooperative breeding through group augmentation. Proc R Soc Lond B 268:187–196

    CAS  Article  Google Scholar 

  30. Konovalov DA, Manning C, Henshaw MT (2004) KINGROUP: a program for pedigree relationship reconstruction and kin group assignments using genetic markers. Mol Ecol Notes 4:779–782

    Article  Google Scholar 

  31. Kopps AM, McDonald PG, Rollins LA (2013) Isolation and characterisation of polymorphic microsatellite loci for noisy miners Manorina melanocephala, with successful cross-amplification in bell miners M. melanophrys. Conserv Genet Res 5:39–41

    Article  Google Scholar 

  32. Lehmann L, Keller L (2006) The evolution of cooperation and altruism ­ a general framework and a classification of models. J Evol Biol 19:1365–1376

  33. Leseberg NP, Lambert KTA, McDonald PG (2015) Fine-scale impacts on avian biodiversity due to a despotic species, the bell miner (Manorina melanophrys). Austral Ecol 40:245–254

    Article  Google Scholar 

  34. Ligon JD, Ligon SH (1983) Reciprocity in the green woodhoopoe (Phoeniculus purpurens). Anim Behav 31:480–489

    Article  Google Scholar 

  35. Loyn RH, Runnalls RG, Forward GY (1983) Territorial bell miners and other birds affecting populations of insect prey. Science 221:1411–1413

    PubMed  CAS  Article  Google Scholar 

  36. Madden J, Nielsen J, Clutton-Brock TH (2012) Do networks of social interactions reflect patterns of kinship? Curr Zool 58:319–328

    Google Scholar 

  37. McDonald D (2009) Young-boy networks without kin clusters in a lek-mating manakin. Behav Ecol Sociobiol 63:1029–1034

    Article  Google Scholar 

  38. McDonald PG (2012) Cooperative bird differentiates between the calls of different individuals, even when vocalizations were from completely unfamiliar individuals. Biol Lett 8:365–368

    PubMed  PubMed Central  Article  Google Scholar 

  39. McDonald PG (2014) Cooperative breeding beyond kinship: why else do helpers help? Emu 114:91–96

    Google Scholar 

  40. McDonald PG, Heathcote CF, Clarke MF, Wright J, Kazem AJN (2007a) Provisioning calls of the cooperatively breeding bell miner Manorina melanophrys encode sufficient information for individual discrimination. J Avian Biol 38:113–121

  41. McDonald PG, Kazem AJN, Clarke MF, Wright J (2008) Helping as a signal: does removal of potential audiences alter helper behavior in the bell miner? Behav Ecol 19:1047–1055

    Article  Google Scholar 

  42. McDonald PG, Kazem AJN, Wright J (2007b) A critical analysis of ‘false-feeding’ behaviour in a cooperatively breeding bird: disturbance effects, satiated nestlings or deception? Behav Ecol Sociobiol 61:1623–1635

    Article  Google Scholar 

  43. McDonald PG, Kazem AJN, Wright J (2009) Cooperative provisioning dynamics: fathers and unrelated helpers show similar responses to manipulations of begging. Anim Behav 77:369–376

    Article  Google Scholar 

  44. McDonald PG, Wright J (2011) Bell miner provisioning calls are more similar among relatives and are used by helpers at the nest to bias their effort towards kin. Proc R Soc Lond B 278:3403–3411

    Article  Google Scholar 

  45. Mehdiabadi NJ, Jack CN, Farnham TT, Platt TG, Kalla SE, Shaulsky G, Queller DC, Strassmann JE (2006) Kin preference in a social microbe. Nature 442:881–882

    PubMed  CAS  Article  Google Scholar 

  46. Painter JN, Crozier RH, Poiani A, Robertson RJ, Clarke MF (2000) Complex social organization reflects genetic structure and relatedness in the cooperatively breeding bell miner, Manorina melanophrys. Mol Ecol 9:1339–1347

  47. Poiani A (1993) Social structure and the development of helping behaviour in the bell miner (Manorina melanophrys, Meliphagidae). Ethology 93:62–80

    Article  Google Scholar 

  48. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org/

  49. Radford AN (2005) Group-specific vocal signatures and neighbour–stranger discrimination in the cooperatively breeding green woodhoopoe. Anim Behav 70:1227–1234

    Article  Google Scholar 

  50. Rollins LA, Browning LE, Holleley CE, Savage JL, Russell AF, Griffith SC (2012) Building genetic networks using relatedness information: a novel approach for the estimation of dispersal and characterization of group structure in social animals. Mol Ecol 21:1727–1740

    PubMed  Article  Google Scholar 

  51. Russell AF, Hatchwell BJ (2001) Experimental evidence for kin biased helping in a cooperatively breeding vertebrate. Proc R Soc Lond B 268:2169–2174

  52. Russell AF, Sharpe LL, Brotherton PNM, Clutton-Brock TH (2003) Cost minimization by helpers in cooperative vertebrates. Proc Natl Acad Sci U S A 100:3333–3338

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  53. Sharp SP, McGowan A, Wood MJ, Hatchwell BJ (2005) Learned kin recognition cues in a social bird. Nature 434:1127–1130

    PubMed  CAS  Article  Google Scholar 

  54. Shizuka D, Chaine AS, Anderson J, Johnson O, Laursen IM, Lyon BE (2014) Across-year social stability shapes network structure in wintering migrant sparrows. Ecol Lett 8:998–1007

    Article  Google Scholar 

  55. Sih A, Hanser S, McHugh K (2009) Social network theory: new insights and issues for behavioral ecologists. Behav Ecol Sociobiol 63:975–988

    Article  Google Scholar 

  56. te Marvelde L, McDonald PG, Kazem AJN, Wright J (2009) Do helpers really help? Provisioning biomass and prey type effects on nestling growth in the cooperative bell miner. Anim Behav 77:727–735

    Article  Google Scholar 

  57. Tibbetts EA, Dale J (2007) Individual recognition: it is good to be different. Trends Ecol Evol 22:529–537

    PubMed  Article  Google Scholar 

  58. Warrington MH, McDonald PG, Griffith SC (2015) Within-group vocal differentiation of individuals in the cooperatively breeding apostlebird. Behav Ecol 26:493–501

    Article  Google Scholar 

  59. West SA, El Mouden C, Gardner A (2011) Sixteen common misconceptions about the evolution of cooperation in humans. Evol Hum Behav 32:231–262

    Article  Google Scholar 

  60. Whitehead H (2008) Analyzing animal societies: quantitative methods for vertebrate social analysis. University of Chicago Press, Chicago

    Google Scholar 

  61. Woolfenden GE, Fitzpatrick JW (1978) The inheritance of territory in group-breeding birds. Bioscience 28:104–108

    Article  Google Scholar 

  62. Wright J (2007) Cooperation theory meets cooperative breeding: exposing some ugly truths about social prestige, reciprocity and group augmentation. Behav Process 76:142–148

    Article  Google Scholar 

  63. Wright J, McDonald PG (in press) Sex, showing-off and relatedness in helping decisions of the cooperatively breeding bell miner. In: Koenig W, Dickinson J (eds) Cooperative breeding: studies of ecology, evolution, and behavior. Cambridge University Press, Cambridge

  64. Wright J, McDonald PG, te Marvelde L, Kazem AJN, Bishop C (2010) Helping effort increases with relatedness in bell miners, but ‘unrelated’ helpers of both sexes still provide substantial care. Proc R Soc Lond B 277:437–445

    Article  Google Scholar 

  65. Wright J, Parker PG, Lundy KJ (1999) Relatedness and chick-feeding effort in the cooperatively breeding Arabian babbler. Anim Behav 58:779–785

    PubMed  Article  Google Scholar 

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Acknowledgments

Nick and Joan Hoogenraad and the La Trobe University Wildlife Reserve kindly allowed fieldwork on their land. Maria Pacheco, Luc te Marvelde and Jonathon Wright assisted with fieldwork. Simon Griffith provided facilities for molecular analyses, with Anna Kopps and Serena Lam assisting with laboratory work. We thank two anonymous reviewers, Prof. Theo Bakker and Dr. Bernhard Voelkl for providing helpful comments on earlier drafts. LAR was funded through an ARC Discovery Project grant to Simon Griffith at Macquarie University (DP1094295), SG through a Discovery Early Career Researcher Award from the Australian Research Council (DE120101470) and PM by the University of New England and a Biotechnology and Biological Sciences Research Council grant to Jonathan Wright at Bangor University (5/S19268).

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All applicable international, national and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. This article does not contain any studies with human participants performed by any of the authors. Research was approved by the La Trobe University Animal Ethics committee (AEC01/19(L)/V2), the Department of Sustainability and Environment (licence 10002082) and the Australian Bird and Bat Banding Scheme (A2259), who also provided leg bands.

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Communicated by B. Voelkl

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McDonald, P.G., Rollins, L.A. & Godfrey, S. The relative importance of spatial proximity, kin selection and potential ‘greenbeard’ signals on provisioning behaviour among helpers in a cooperative bird. Behav Ecol Sociobiol 70, 133–143 (2016). https://doi.org/10.1007/s00265-015-2032-8

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Keywords

  • Cooperative breeding
  • Direct benefits
  • Inclusive fitness
  • Indirect benefits
  • Population viscosity
  • Social networks analysis