Skip to main content
SpringerLink
Log in

Kin associations and direct vs indirect fitness benefits in colonial cooperatively breeding sociable weavers Philetairus socius

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Indirect fitness benefits are believed to be an important force behind the evolution of cooperative breeding. However, helpers may associate with their relatives as a result of delayed dispersal, hence, kin associations might be a consequence of demographic viscosity rather than active choice. In addition, recent studies showed that helpers may have access to reproduction therefore direct benefits might also play an important role. Here, we investigate the possible roles of direct genetic benefits and kin associations on helping behavior in the sociable weaver Philetairus socius, a colonial and cooperatively breeding passerine. We used a microsatellite-based genotyping method to describe the genetic structure within nests and colonies. Within a colony, we found considerable genetic structure between males but not females. Sociable weaver colonies have several nests that are simultaneously active, giving individuals a choice of associating with a range of first-order kin to unrelated individuals. Helpers were significantly more related to the young in the helped nests than in other nests of the colony, suggesting an active choice for associating with kin. The helpers were generally offspring or first-order relatives of one (50%) or both (43%) breeders, although more infrequently, seemingly unrelated individuals also helped (7%). We found no supporting evidence of extrapair parentage and hence no direct genetic gains from helping in our population. This strong reproductive skew is contrary to theoretical models predicting conflicts over reproduction in stepfamilies. We discuss whether female decisions and/or other direct benefits of remaining in kin associations or helping might explain the high skew observed.

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

  • Baglione V, Canestrari D, Marcos JM, Ekman J (2003) Kin selection on cooperative alliances of carrion crows. Science 300:1947–1949

    Article  PubMed  CAS  Google Scholar 

  • Canestrari D, Marcos JM, Baglione V (2005) Effect of parentage and relatedness on the individual contributions to cooperative chick care in the carrion crow Corvus corone corone. Behav Ecol Sociobiol 57:422–428

    Article  Google Scholar 

  • Cant MA (1998) A model for the evolution of reproductive skew without reproductive suppression. Anim Behav 55:163–169

    Article  PubMed  Google Scholar 

  • Chao L (1997) Evolution of polyandry in a communal breeding system. Behav Ecol 8:668–674

    Article  Google Scholar 

  • Chomczynski P, Mackey K, Drews R, Wilfinger W (1997) DNAzol: a reagent for the rapid isolation of genomic DNA. Biotechniques 22:550–553

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Clutton-Brock TH, Gaynor D, McIlrath GM, MacColl ADC, Kansky R, Chadwick C, Manser M, Skinner JD, Brotherton PNM (1999) Predation, group size and mortality in a cooperative mangoose, Suricata suricatta. J Anim Ecol 68:672–683

    Article  Google Scholar 

  • Clutton-Brock TH, Brotherton PNM, O’Riain MJ, Griffin AS, Gaynor D, Kansky R, Sharpe LL, McIlrath GM (2001) Contributions to cooperative rearing in meerkats, Suricata suricatta. Anim Behav 61:705–710

    Article  Google Scholar 

  • Cockburn A (1998) Evolution of helping behaviour in cooperatively breeding birds. Ann Rev Ecolog Syst 29:141–177

    Article  Google Scholar 

  • Cockburn A (2004) Mating systems and sexual conflict. In: Koenig WD, Dickinson JL (eds) Ecology and evolution of cooperative breeding in birds. Cambridge Univ. Press, Cambridge, pp 81–101

    Google Scholar 

  • Covas R (2002) Life history evolution and cooperative breeding in the sociable weaver. In: Percy FitzPatrick Institute. University of Cape Town, Cape Town

  • Covas R, du Plessis MA (2005) The effect of helpers on artificially increased brood size in sociable weavers (Philetairus socius). Behav Ecol Sociobiol 57:631–636

    Article  Google Scholar 

  • Covas R, Doutrelant C, du Plessis MA (2004) Experimental evidence of a link between breeding conditions and the decision to breed or to help in a colonial cooperative breeder. Proc R Soc Lond B 271:827–832

    Article  Google Scholar 

  • Dickinson JL (2003) Male share of provisioning is not influenced by actual or apparent loss of paternity in western bluebirds. Behav Ecol 14:360–366

    Article  Google Scholar 

  • Dickinson JL (2004) A test of the importance of direct and indirect fitness benefits for helping decisions in western bluebirds. Behav Ecol 15:233–238

    Article  Google Scholar 

  • Don RH, Cox PT, Wainwright BJ, Baker K, Mattick JS (1991) Touchdown PCR to circumvent spurious priming during gene amplification. Nucleic Acid Res 19:4008

    Article  PubMed  CAS  Google Scholar 

  • Doutrelant C, Covas R, Caizergues A, du Plessis MA (2004) Unexpected sex ratio adjustment in a colonial cooperative bird: pairs with helpers produce more of the helping sex whereas pairs without helpers do not. Behav Ecol Sociobiol 56:149–154

    Article  Google Scholar 

  • Dunn PO, Cockburn A (1999) Extra-pair mate choice and honest signaling in cooperatively breeding superb fairy-wrens. Evolution 53:938–946

    Article  Google Scholar 

  • Ekman J, Bylin A, Tegelström H (1999) Increased lifetime reproductive success for Siberian jay (Perisoreus infaustus) males with delayed dispersal. Proc R Soc Lond B 266:911–915

    Article  Google Scholar 

  • Ekman J, Bylin A, Tegelström H (2000) Parental nepotism enhances survival of retained offspring in the Siberian jay. Behav Ecol 11:416–420

    Article  Google Scholar 

  • Ekman J, Baglione V, Eggers S, Griesser M (2001) Delayed dispersal: living under the reign of nepotistic parents. Auk 118:1–10

    Article  Google Scholar 

  • Emlen ST (1997) Predicting family dynamics in social vertebrates. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach, 4th edn. Blackwell Science, Cambridge, pp 228–253

    Google Scholar 

  • Goodnight KF (2000) Relatedness 5.0. Goodnight software. Houston, Texas

  • Green DJ, Cockburn A (2001) Post-fledging care, philopatry and recruitment in brown thornbills. J Anim Ecol 70:505–514

    Article  Google Scholar 

  • Griffin AS, West SA (2002) Kin selection: fact and fiction. Trends Ecol Evol 17:15–21

    Article  Google Scholar 

  • Griffin AS, West SA (2003) Kin discrimination and the benefit of helping in cooperatively breeding vertebrates. Science 302:634–636

    Article  PubMed  CAS  Google Scholar 

  • Griffith SC, Stewart IRK, Dawson DA, Owens IPF, Burke T (1999) Contrasting levels of extra-pair paternity in island and mainland populations of the house sparrow (Passer domesticus): is there an island effect? Biol J Linn Soc 68:303–316

    Google Scholar 

  • Griffith SC, Owens IPF, Thuman KA (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212

    Article  PubMed  CAS  Google Scholar 

  • Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Heinsohn R, Dunn PO, Legge S, Double MC (2000) Coalitions of relatives and reproductive skew in cooperatively breeding white-winged choughs. Proc R Soc Lond B 267:243–249

    Article  CAS  Google Scholar 

  • Jones AG, Ardren WR (2003) Methods of parentage analysis in natural populations. Mol Ecol 12:2511–2523

    Article  PubMed  CAS  Google Scholar 

  • Keller L, Reeve HK (1994) Partitioning of reproduction in animal societies. Trends Ecol Evol 9:98–102

    Article  Google Scholar 

  • Koenig WD, Pitelka FA (1979) Relatedness and inbreeding avoidance: counter ploys in the communally nesting acorn woodpecker. Science 206:1103–1105

    Article  PubMed  Google Scholar 

  • Koenig WD, Stanback MT, Haydock J (1999) Demographic consequences of incest avoidance in the cooperatively breeding acorn woodpecker. Anim Behav 57:1287–1293

    Article  PubMed  Google Scholar 

  • Komdeur J (1996) Influence of helping and breeding experience on reproductive performance in the Seychelles warbler: a translocation experiment. Behav Ecol 7:326–333

    Article  Google Scholar 

  • Legge S, Cockburn A (2000) Social and mating system of cooperatively breeding laughing kookaburras (Dacelo novaeguineae). Behav Ecol Sociobiol 47:220–229

    Article  Google Scholar 

  • Lessells CM, Avery MI, Krebs JR (1994) Nonrandom dispersal of kin—why do European bee-eaters (Merops apiaster) brothers nest close together. Behav Ecol 5:105–113

    Article  Google Scholar 

  • Maclean GL (1973a) The sociable weaver, part 1: description, distribution, dispersion and populations. Ostrich 44:176–190

    Google Scholar 

  • Maclean GL (1973b) The sociable weaver, part 2: nest architecture and social organisation. Ostrich 44:191–218

    Google Scholar 

  • Magrath RD, Heinsohn R (2000) Reproductive skew in birds: models, problems and prospects. J Avian Biol 31:247–258

    Article  Google Scholar 

  • Magrath RD, Whittingham LA (1997) Subordinate males are more likely to help if unrelated to the breeding female in cooperatively breeding white-browed scrubwrens. Behav Ecol Sociobiol 41:185–192

    Article  Google Scholar 

  • Marsden RM (1999) Coloniality in the sociable weaver Philetairus socius. In: Animal and plant sciences. Sheffield University, Sheffield, pp 104

    Google Scholar 

  • Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

    Article  PubMed  CAS  Google Scholar 

  • McRae SB, Amos W (1999) Characterization of hypervariable microsatellites in the cooperatively breeding white-browed sparrow weaver Plocepasser mahali. Mol Ecol 8:903–904

    PubMed  CAS  Google Scholar 

  • Mendelsohn JM, Anderson MD (1997) Sociable weaver Philetairus socius. In: Harrison JA, Allan DG, Underhill LG, Herremans M, Tree AJ, Parker V, Brown CJ (eds) The atlas of Southern African birds. Birdlife South Africa, Johannesburg, pp 534–535

    Google Scholar 

  • Møller AP, Birkhead TR (1993) Certainty of paternity covaries with paternal care in birds. Behav Ecol Sociobiol 33:261–268

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Putland D (2001) Has sexual selection been overlooked in the study of avian helping behaviour? Anim Behav 62:811–814

    Article  Google Scholar 

  • Queller DC, Goodnight KF (1989) Estimation of genetic relatedness using allozyme data. Evolution 43:258–275

    Article  Google Scholar 

  • Queller DC, Strassman JE, Hughes CR (1993) Microsatellites and kinship. Trends Ecol Evol 8:285–288

    Article  Google Scholar 

  • Quinn JS, Woolfenden GE, Fitzpatrick JW, White BN (1999) Multi-locus DNA fingerprinting supports genetic monogamy in Florida scrub-jays. Behav Ecol Sociobiol 45:1–10

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Richardson DS, Jury FL, Blaakmeer K, Komdeur J, Burke T (2001) Parentage assignment and extra-group paternity in a cooperative breeder: the Seychelles warbler (Acrocephalus Sechellensis). Mol Ecol 10:2263–2273

    Article  PubMed  CAS  Google Scholar 

  • Richardson DS, Burke T, Komdeur J (2002) Direct benefits and the evolution of female-biased cooperative breeding in the Seychelles warblers. Evolution 56:2313–2321

    PubMed  Google Scholar 

  • Richardson DS, Burke T, Komdeur J (2003) Sex-specific associative learning cues and inclusive fitness benefits in the Seychelles warbler. J Evol Biol 16:854–861

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sheldon BC (2002) Relating paternity to paternal care. Philos Trans R Soc Lond B Biol Sci 357:341–350

    Article  PubMed  Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry. Freeman, New York

    Google Scholar 

  • Stacey PB, Koenig WD (1990) Cooperative breeding in birds. Cambridge Univ. Press, Cambridge

    Google Scholar 

  • Vehrencamp SL (2000) Evolutionary routes to joint-female nesting in birds. Behav Ecol 11:334–344

    Article  Google Scholar 

  • Webster MS, Tarvin KA, Tuttle EM, Pruett-Jones S (2004) Reproductive promiscuity in the splendid fairy-wren: effects of group size and auxiliary reproduction. Behav Ecol 15:907–915

    Article  Google Scholar 

  • Whittingham L, Dunn PO, Magrath RD (1997) Relatedness, polyandry and extragroup paternity in the cooperatively breeding white-browed scrubwren (Sericornis frontalis). Behav Ecol Sociobiol 40:261–270

    Article  Google Scholar 

  • Winterbottom M, Burke T, Birkhead TR (2001) The phalloid organ, orgasm, and sperm competition in a polygynandrous bird: the red-billed buffalo weaver (Bubalornis niger). Behav Ecol Sociobiol 50:474–482

    Article  Google Scholar 

  • Zahavi A (1995) Altruism as an handicap—the limitations of kin selection and reciprocity. J Avian Biol 26:1–3

    Article  Google Scholar 

Download references

Acknowledgements

We are very grateful to the numerous field helpers that assisted us over the years. We thank M. A. du Plessis for advice and discussion at different stages of the study and D. S. Richardson for advice regarding the parentage analyses. Comments from two anonymous referees greatly improved a previous version of the manuscript. Mark Anderson provided helpful advice in the field and help with logistic problems. For help with lab work, we thank E. Tack, M. P. Melo, and C. Brouat. The lab work was conducted at the CBGP, Montpellier (in A. Estoup’s group). De Beers Consolidated Mining Corp. gave us access to Benfontein Game Farm where the work was conducted. C. D. was funded by a postdoctoral grant from the South African Research Foundation during the field and lab work. R. C. and the lab work were funded by program Praxis XXI (BD 11497/97; FCT, Portugal). Additional funding during the writing stage was provided by the exchange program Alliance (France) to R. C. and C. D. The work was conducted with the permission of Northern Cape Nature Conservation and the Ethics Committee of the University of Cape Town.

Author information

Authors and Affiliations

  1. Percy FitzPatrick Institute, Department of Science and Technology (DST) Centre of Excellence, University of Cape Town, Rondebosch, 7701, South Africa

    Rita Covas & Claire Doutrelant

  2. Institute of Evolutionary Biology, University of Edinburgh, West Mains Road, Edinburgh, EH9 3JT, UK

    Rita Covas

  3. Unidade de Macroecologia e Conservação, Centro de Ecologia Aplicada (CEA), Universidade de Évora, Largo dos Colegiais 2, Évora, 7002-554, Portugal

    Rita Covas

  4. Institut National de la Recherche Agronomique (INRA), UMR Centre de Biologie et de Gestion des Populations (CBGP), Campus international de Baillarguet, CS 30016, Montferrier-sur-Lez cedex, 34 988, France

    Ambroise Dalecky

  5. Office National de la Chasse et de la Faune Sauvage (ONCFS), Direction des Etudes et de la Recherche, Centres nationaux d’Etudes et de Recherche appliquée (CNERA) AM, 53, Rue Russeil, Nantes, 44000, France

    Alain Caizergues

  6. Centre d’Ecologie Fonctionnelle et Evolutive, Centre National de la Recherche Scientifique (CEFE-CNRS), 1919 Route de Mende, Montpellier Cedex 5, 34293, France

    Claire Doutrelant

Authors
  1. Rita Covas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ambroise Dalecky
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alain Caizergues
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Claire Doutrelant
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rita Covas.

Additional information

Communicated by A. Cockburn

Rights and permissions

Reprints and permissions

About this article

Cite this article

Covas, R., Dalecky, A., Caizergues, A. et al. Kin associations and direct vs indirect fitness benefits in colonial cooperatively breeding sociable weavers Philetairus socius . Behav Ecol Sociobiol 60, 323–331 (2006). https://doi.org/10.1007/s00265-006-0168-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-006-0168-2

Keywords

Search

Navigation