Behavioral Ecology and Sociobiology

, Volume 69, Issue 11, pp 1835–1843 | Cite as

Relatedness predicts multiple measures of investment in cooperative nest construction in sociable weavers

  • Gavin M. Leighton
  • Sebastian Echeverri
  • Dirk Heinrich
  • Holger Kolberg
Original Article

Abstract

Although communal goods are often critical to society, they are simultaneously susceptible to exploitation and are evolutionarily stable only if mechanisms exist to curtail exploitation. Mechanisms such as punishment and kin selection have been offered as general explanations for how communal resources can be maintained. Evidence for these mechanisms comes largely from humans and social insects, leaving their generality in question. To assess how communal resources are maintained, we observed cooperative nest construction in sociable weavers (Philetairus socius). The communal nest of sociable weavers provides thermal benefits for all individuals but requires continual maintenance. We observed cooperative nest construction and also recorded basic morphological characteristics. We also collected blood samples, performed next-generation sequencing, and isolated 2358 variable single nucleotide polymorphisms (SNPs) to estimate relatedness. We find that relatedness predicts investment in cooperative nest construction, while no other morphological characters significantly explain cooperative output. We argue that indirect benefits are a critical fitness component for maintaining the cooperative behavior that maintains the communal good.

Keywords

Sociable weavers Kin selection Inclusive fitness Tragedy of the commons Cooperation 

Supplementary material

265_2015_1996_MOESM1_ESM.docx (505 kb)
ESM 1(DOCX 504 kb)

References

  1. Allen B, Nowak MA, Wilson EO (2013) Limitations of inclusive fitness. P Natl Acad Sci USA 110:20135–20139CrossRefGoogle Scholar
  2. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135CrossRefPubMedGoogle Scholar
  3. Boomsma JJ (2009) Lifetime monogamy and the evolution of eusociality. Proc R Soc Lond B 364:3191–3207Google Scholar
  4. Bourke AFG (2011a) Principles of social evolution. Oxford University Press, OxfordCrossRefGoogle Scholar
  5. Bourke AFG (2011b) The validity and value of inclusive fitness theory. Proc R Soc Lond B 282:1–9Google Scholar
  6. 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 279:3861–3869CrossRefGoogle Scholar
  7. Burnham KP, Anderson DR, Huyvaert KP (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65:23–35CrossRefGoogle Scholar
  8. Canestrari D, Marcos JM, Baglione V (2005) Effect of parentage and relatedness on the individual contribution to cooperative chick care in carrion crows Corvus corone corone. Behav Ecol Sociobiol 57:422–428CrossRefGoogle Scholar
  9. Clutton-Brock T, Brotherton PNM, Russel AF et al (2001) Cooperation, control, and concession in meerkat groups. Science 291:478–481CrossRefPubMedGoogle Scholar
  10. Clutton-Brock T, Russell A, Sharpe L, Young A, Balmforth Z, McIlrath G (2002) Evolution and development of sex differences in cooperative behavior in meerkats. Science 297:253–256CrossRefPubMedGoogle Scholar
  11. Collias NE, Victoria JK (1978) Nest and mate selection in the village weaverbird. Anim Behav 26:470–479CrossRefGoogle Scholar
  12. Connor RC (2010) Cooperation beyond the dyad: on simple models and a complex society. Proc R Soc Lond B 365:2687–2697Google Scholar
  13. Cornwallis CK, West SA, Davis KE, Griffin AS (2010) Promiscuity and the evolutionary transition to complex societies. Nature 466:969–972CrossRefPubMedGoogle Scholar
  14. Covas R, Dalecky A, Caizergues A, Doutrelant C (2006) Kin associations and direct vs indirect fitness benefits in colonial cooperatively breeding sociable weavers Philetairus socius. Behav Ecol Sociobiol 60:323–331CrossRefGoogle Scholar
  15. Covas R, Doutrelant C, du Plessis M (2004) Experimental evidence of a link between breeding conditions and the decision to breed or to help in a colonial cooperative bird. Proc R Soc Lond B 271:827–832CrossRefGoogle Scholar
  16. Doutrelant C, Covas R (2007) Helping has signalling characteristics in a cooperatively breeding bird. Anim Behav 74:739–747CrossRefGoogle Scholar
  17. Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6:e19379PubMedCentralCrossRefPubMedGoogle Scholar
  18. Fisher R, Cornwallis CK, West S (2013) Group formation, relatedness and the evolution of multicellularity. Curr Biol 23:1120–1125CrossRefPubMedGoogle Scholar
  19. Frank S (1995) Mutual policing and repression of competition in the evolution of cooperative groups. Nature 377:520–522CrossRefPubMedGoogle Scholar
  20. Frank S (2010) A general model of the public goods dilemma. J Evol Biol 23:1245–1250PubMedCentralCrossRefPubMedGoogle Scholar
  21. Glaubitz JC, Casstevens T, Lu F, Harriman J, Elshire RJ, Sun Q, Buckler ES (2014) TASSEL-GBS: a high capacity genotyping by sequencing analysis pipeline. PLoS One 9:e90346PubMedCentralCrossRefPubMedGoogle Scholar
  22. Grafen A (1985) A geometric view of relatedness. Oxf Surv Evol Biol 2:28–90Google Scholar
  23. Griffiths R, Double M, Orr K, Dawson R (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075CrossRefPubMedGoogle Scholar
  24. Hamilton W (1964) Genetical evolution of social behaviour I. J Theor Biol 7:1–16CrossRefPubMedGoogle Scholar
  25. Han J-I, Kim J-H, Kim S, Park S-R, Na K-J (2009) A simple and improved DNA test for avian sex determination. Auk 126:779–783CrossRefGoogle Scholar
  26. Hardin G (1968) Tragedy of the commons. Science 162:1243CrossRefPubMedGoogle Scholar
  27. Hölldobler B, Wilson EO (1990) The ants. Belknap, CambridgeCrossRefGoogle Scholar
  28. Hughes WOH, Oldroyd BP, Beekman M, Ratnieks FLW (2008) Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320:1213–1216CrossRefPubMedGoogle Scholar
  29. Jackson D (2007) Social spiders. Curr Biol 17:R650–R652CrossRefPubMedGoogle Scholar
  30. Johnson Brian R, Borowiec Marek L, Chiu Joanna C, Lee Ernest K, Atallah J, Ward Philip S (2013) Phylogenomics resolves evolutionary relationships among ants, bees, and wasps. Curr Biol 23:2058–2062CrossRefPubMedGoogle Scholar
  31. Johnstone RA, Cant MA (2008) Sex differences in dispersal and the evolution of helping and harming. Am Nat 172:318–330CrossRefPubMedGoogle Scholar
  32. Lacey E, Sherman PW (1991) Social organization of naked mole-rat colonies: evidence for divisions of labor. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The biology of the naked mole-rat. Princeton University Press, Princeton, New Jersey, pp 275–336Google Scholar
  33. Lehmann L (2007) The evolution of trans-generational altruism: kin selection meets niche construction. J Evol Biol 20:181–189CrossRefPubMedGoogle Scholar
  34. Leigh EG (2010) The group selection controversy. J Evol Biol 23:6–19CrossRefPubMedGoogle Scholar
  35. Leighton GM (2014a) The relative effectiveness of signaling systems: relying on external items reduces signaling accuracy while leks increase accuracy. PLoS One 9:e91725PubMedCentralCrossRefPubMedGoogle Scholar
  36. Leighton GM (2014b) Sex and individual differences in cooperative nest construction of sociable weavers. J Ornithol 155:927–935CrossRefGoogle Scholar
  37. Leighton GM, Echeverri S (2014) Non-linear influence of nest size on thermal buffering of sociable weaver nests and the maintenance of cooperative nest construction. Avian Biol Res 7:255–260CrossRefGoogle Scholar
  38. Leighton GM, Echeverri S (2015) Stable isotope signatures reveal cryptic differences in diet of sociable weavers. Avian Biol Res 8:104–108Google Scholar
  39. Lessells C, Boag P (1987) Unrepeatable repeatabilities—a common mistake. Auk 104:116–121CrossRefGoogle Scholar
  40. Lukas D, Clutton-Brock T (2012) Cooperative breeding and monogamy in mammalian societies. Proc R Soc Lond B 279:2151–2156CrossRefGoogle Scholar
  41. Maclean G (1973) The sociable weaver (parts 1-5). Ostrich 44:176–216CrossRefGoogle Scholar
  42. Maynard Smith J, Szathmáry E (1995) The major transitions in evolution. Oxford University Press, OxfordGoogle Scholar
  43. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956PubMedGoogle Scholar
  44. Nakagawa S, Schielzeth H, O'Hara RB (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142CrossRefGoogle Scholar
  45. Napper CJ, Sharp SP, McGowan A, Simeoni M, Hatchwell BJ (2013) Dominance, not kinship, determines individual position within the communal roosts of a cooperatively breeding bird. Behav Ecol Sociobiol 67:2029–2039CrossRefGoogle Scholar
  46. Nowak MA, Tarnita CE, Wilson EO (2010) The evolution of eusociality. Nature 466:1057–1062PubMedCentralCrossRefPubMedGoogle Scholar
  47. Price JJ, Whalen LM (2009) Plumage evolution in the oropendolas and caciques: different divergence rates in polygynous and monogamous taxa. Evolution 63:2985–2998CrossRefPubMedGoogle Scholar
  48. Pruitt JN, Riechert SE (2009) Frequency dependent success of cheaters during foraging bouts might limit their spread within colonies of a socially polymorphic spider. Evolution 63:2966–2973CrossRefPubMedGoogle Scholar
  49. Quader S (2006) What makes a good nest? benefits of nest choice to female baya weavers (Ploceus philippinus). Auk 123:475–486CrossRefGoogle Scholar
  50. Queller DC, Strassmann JE (1998) Kin selection and social insects. Bioscience 48:165–175Google Scholar
  51. Queller DC, Strassmann JE (2009) Beyond society: the evolution of organismality. Proc Rev Soc Lond B 364:3143–3155Google Scholar
  52. Rankin DJ, Bargum K, Kokko H (2007) The tragedy of the commons in evolutionary biology. Trends Ecol Evol 22:643–651CrossRefPubMedGoogle Scholar
  53. Rat M, van Dijk RE, Covas R, Doutrelant C (2015) Dominance hierarchies and associated signalling in a cooperative passerine. Behav Ecol Sociobiol 69:437–448CrossRefGoogle Scholar
  54. Richards SA, Whittingham MJ, Stephens PA (2011) Model selection and model averaging in behavioural ecology: the utility of the IT-AIC framework. Behav Ecol Sociobiol 65:77–89CrossRefGoogle Scholar
  55. Rousset F, Lion S (2011) Much ado about nothing: Nowak et al.’s charge against inclusive fitness theory. J Evol Biol 24:1386–1392CrossRefPubMedGoogle Scholar
  56. Rubenstein DR, Lovette IJ (2009) Reproductive skew and selection on female ornamentation in social species. Nature 462:786–789CrossRefPubMedGoogle Scholar
  57. Sherman PW (1981) Kinship, demography, and Belding’s ground squirrel nepotism. Behav Ecol Sociobiol 8:251–259CrossRefGoogle Scholar
  58. Strassmann JE, Queller DC (2010) The social organism: congresses, parties, and committees. Evolution 64:605–616CrossRefPubMedGoogle Scholar
  59. Strassmann JE, Queller DC (2011) Evolution of cooperation and control of cheating in a social microbe. P Natl Acad Sci USA 108:10855–10862CrossRefGoogle Scholar
  60. Thompson EA (1975) The estimation of pairwise relationships. Ann Hum Genet 39:173–188CrossRefPubMedGoogle Scholar
  61. Traulsen A (2010) Mathematics of kin- and group selection: formally equivalent? Evolution 64:316–323CrossRefPubMedGoogle Scholar
  62. van Dijk R, Kaden JC, Argüelles‐Tico A, Beltran M, Paquet M, Covas R, Doutrelant C, Hatchwell BJ (2013) The thermoregulatory benefits of the communal nest of sociable weavers Philetairus socius are spatially structured within nests. J Avian Biol 44:102–110CrossRefGoogle Scholar
  63. van Dijk R, Kaden JC, Arguelles-Tico A, Dawson DA, Burke T, Hatchwell BJ (2014) Cooperative investment in public goods is kin directed in communal nests of social birds. Ecol Lett 17:1141–1148PubMedCentralCrossRefPubMedGoogle Scholar
  64. West SA, Gardner A (2013) Adaptation and inclusive fitness. Curr Biol 23:R577–R584CrossRefPubMedGoogle Scholar
  65. West SA, Gardner A, Shuker D, Reynolds T, Burton-Chellow M, Sykes E, Guinnee M, Griffin A (2006) Cooperation and the scale of competition in humans. Curr Biol 16:1103–1106CrossRefPubMedGoogle Scholar
  66. West SA, Pen I, Griffin A (2002) Conflict and cooperation—cooperation and competition between relatives. Science 296:72–75CrossRefPubMedGoogle Scholar
  67. Wilson DS, Wilson EO (2007) Rethinking the theoretical foundation of sociobiology. Q Rev Biol 82:327–348CrossRefPubMedGoogle Scholar
  68. Wright J, McDonald PG, te Marvelde L, Kazem AJN, Bishop CM (2010) Helping effort increases with relatedness in bell miners, but ‘unrelated’ helpers of both sexes still provide substantial care. Proc R Soc Lond B 277:437–445CrossRefGoogle Scholar
  69. Zhang Y (2013) Likelihood-based and Bayesian methods for Tweedie compound Poisson linear mixed models. Stat Comput 23:743–757CrossRefGoogle Scholar
  70. Zheng X, Levine D, Shen J, Gogarten SM, Laurie C, Weir BS (2012) A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics 28:3326–3328PubMedCentralCrossRefPubMedGoogle Scholar
  71. Zottl M, Heg D, Chervet N, Taborsky M (2013) Kinship reduces alloparental care in cooperative cichlids where helpers pay-to-stay. Nat Commun 4:1–9CrossRefGoogle Scholar
  72. Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Gavin M. Leighton
    • 1
  • Sebastian Echeverri
    • 2
  • Dirk Heinrich
    • 3
  • Holger Kolberg
    • 3
  1. 1.Department of Ecology & Evolutionary BiologyUniversity of ArizonaTucsonUSA
  2. 2.Department of Ecology and EvolutionUniversity of PittsburghPittsburghUSA
  3. 3.SAFRING: Namibian Ringing UnitWindhoekNamibia

Personalised recommendations