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.
Similar content being viewed by others
References
Arnold KE, Owens IPF, Goldizen AW (2005) Division of labour within cooperatively breeding groups. Behaviour 142:1577–1590
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
Bergmüller R, Johnstone RA, Russell AF, Bshary R (2007) Integrating cooperative breeding into theoretical concepts of cooperation. Behav Process 76:61–72
Brown JL (1987) Helping and communal breeding in birds: ecology and evolution. Princeton University Press, Princeton, New Jersey
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
Butts CT (2014) sna: tools for social network analysis. R package version 2.3-2, http://CRAN.R-project.org/package=sna
Clarke MF (1989) The pattern of helping in the bell miner (Manorina melanophrys). Ethology 80:292–306
Clarke MF, Fitz-Gerald GF (1994) Spatial organisation of the cooperatively breeding bell miner Manorina melanophrys. Emu 94:96–105
Clarke MF, Heathcote CF (1990) Dispersal, survivorship and demography in the cooperatively breeding bell miner Manorina melanophrys. Emu 90:15–23
Clauset A, Newman MEJ, Moore C (2004) Finding community structure in very large networks. Phys Rev E 70:066111
Clutton-Brock TH (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296:69–72
Clutton-Brock TH (2009) Cooperation between non-kin in animal societies. Nature 462:51–57
Cockburn A (1998) Evolution of helping behavior in cooperatively breeding birds. Annu Rev Ecol Syst 29:141–177
Connor RC (1986) Pseudo-reciprocity: investing in mutualism. Anim Behav 34:1562–1566
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
Croft DP, James R, Krause J (2008) Exploring animal social networks. Princeton University Press, Princeton, New Jersey
Csardi G, Nepusz T (2006) The igraph software package for complex network research. InterJournal, Complex Systems 1695, http://igraph.org
Dekker D, Krackhard D, Snijders TAB (2007) Sensitivity of MRQAP tests to collinearity and autocorellation conditions. Psychometrika 72:563–581
Farine DR (2013) Animal social network inference and permutations for ecologists in R using asnipe. Meth Ecol Evol 4:1187–1194
Farine DR (2014) Measuring phenotypic assortment in animal social networks: weighted associations are more robust than binary edges. Anim Behav 89:141–153
Gardner A, West SA (2010) Greenbeards. Evolution 64:25–38
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
Hamilton WD (1964) The genetical evolution of social behaviour. II J Theor Biol 7:17–52
Hatchwell BJ (2010) Cryptic kin selection: kin structure in vertebrate populations and opportunities for kin-directed cooperation. Ethology 116:203–216
Heinsohn RG, Legge S (1999) The cost of helping. Trends Ecol Evol 14:53–57
Jetz W, Rubenstein DR (2011) Environmental uncertainty and the global biogeography of cooperative breeding in birds. Curr Biol 21:72–78
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
Khanna H, Gaunt SLL, McCallum DA (1997) Digital spectrographic crosscorrelation: tests of sensitivity. Bioacoustics 7:209–234
Kokko H, Johnstone RA, Clutton-Brock TH (2001) The evolution of cooperative breeding through group augmentation. Proc R Soc Lond B 268:187–196
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
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
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
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
Ligon JD, Ligon SH (1983) Reciprocity in the green woodhoopoe (Phoeniculus purpurens). Anim Behav 31:480–489
Loyn RH, Runnalls RG, Forward GY (1983) Territorial bell miners and other birds affecting populations of insect prey. Science 221:1411–1413
Madden J, Nielsen J, Clutton-Brock TH (2012) Do networks of social interactions reflect patterns of kinship? Curr Zool 58:319–328
McDonald D (2009) Young-boy networks without kin clusters in a lek-mating manakin. Behav Ecol Sociobiol 63:1029–1034
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
McDonald PG (2014) Cooperative breeding beyond kinship: why else do helpers help? Emu 114:91–96
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
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
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
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
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
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
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
Poiani A (1993) Social structure and the development of helping behaviour in the bell miner (Manorina melanophrys, Meliphagidae). Ethology 93:62–80
R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org/
Radford AN (2005) Group-specific vocal signatures and neighbour–stranger discrimination in the cooperatively breeding green woodhoopoe. Anim Behav 70:1227–1234
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
Russell AF, Hatchwell BJ (2001) Experimental evidence for kin biased helping in a cooperatively breeding vertebrate. Proc R Soc Lond B 268:2169–2174
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
Sharp SP, McGowan A, Wood MJ, Hatchwell BJ (2005) Learned kin recognition cues in a social bird. Nature 434:1127–1130
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
Sih A, Hanser S, McHugh K (2009) Social network theory: new insights and issues for behavioral ecologists. Behav Ecol Sociobiol 63:975–988
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
Tibbetts EA, Dale J (2007) Individual recognition: it is good to be different. Trends Ecol Evol 22:529–537
Warrington MH, McDonald PG, Griffith SC (2015) Within-group vocal differentiation of individuals in the cooperatively breeding apostlebird. Behav Ecol 26:493–501
West SA, El Mouden C, Gardner A (2011) Sixteen common misconceptions about the evolution of cooperation in humans. Evol Hum Behav 32:231–262
Whitehead H (2008) Analyzing animal societies: quantitative methods for vertebrate social analysis. University of Chicago Press, Chicago
Woolfenden GE, Fitzpatrick JW (1978) The inheritance of territory in group-breeding birds. Bioscience 28:104–108
Wright J (2007) Cooperation theory meets cooperative breeding: exposing some ugly truths about social prestige, reciprocity and group augmentation. Behav Process 76:142–148
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
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
Wright J, Parker PG, Lundy KJ (1999) Relatedness and chick-feeding effort in the cooperatively breeding Arabian babbler. Anim Behav 58:779–785
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).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical approval
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.
Additional information
Communicated by B. Voelkl
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-015-2032-8