Advertisement

Behavioral Ecology and Sociobiology

, Volume 67, Issue 12, pp 1915–1929 | Cite as

Complete reproductive skew within white-browed sparrow weaver groups despite outbreeding opportunities for subordinates of both sexes

  • Xavier A. Harrison
  • Jennifer E. York
  • Dominic L. Cram
  • Michelle C. Hares
  • Andrew J. YoungEmail author
Original Paper

Abstract

The distribution of reproductive success within societies is a key determinant of the outcomes of social evolution. Attempts to explain social diversity, therefore, require that we quantify reproductive skews and identify the mechanisms that generate them. Here, we address this priority using life history and genotypic data from >600 individuals in 40 wild groups of the cooperatively breeding white-browed sparrow weaver, Plocepasser mahali. We show that groups comprise up to six males and seven females, but within-group reproduction is completely monopolised by a single dominant male and female, while extra-group males sire 12–18 % of offspring. Strong within-group kin structure could frequently explain these monopolies, as subordinates had typically delayed dispersal from their natal groups and so frequently (1) lacked within-group outbreeding partners, and/or (2) stood to gain little from contesting dominant reproduction, being almost as related to the dominant’s young as they would have been to their own. Kin structure alone cannot account entirely for these monopolies, however, as they remained complete following the immigration of unrelated males and females. That subordinate females remain reproductively quiescent despite also showing comparable body condition to dominants, overlapping them substantially in age, and showing no evidence of elevated stress hormone levels raises the possibility that they exercise reproductive restraint due instead to a threat of action by dominants and/or deficits in offspring fitness that might arise if subordinates bred. Our findings highlight the complexity of the mechanisms that generate reproductive disparities in animal societies and the challenge of identifying them when skews are complete.

Keywords

Plocepasser mahali Kin structure Cooperative breeding Reproductive conflict Monogamy Inbreeding avoidance 

Notes

Acknowledgments

We are grateful to our many field assistants during this period (Tom Reed, Brenna Boyle, Andy Mason, Francesca Jarero, Lexy Russell, Padraig Cregg, Lynda Casson, Sam Farrell, Lynda Donaldson, Jenny Sturgeon, and Robyn Silcock) for their tireless efforts under the Kalahari sun, to Northern Cape Conservation for permission to conduct the research, and to E.O. and Son and all at Tswalu Kalahari Reserve for their exceptional logistical support. We thank two anonymous reviewers for helpful comments that improved an earlier draft of this manuscript. This study was funded by a BBSRC David Phillips research fellowship to AY and a NERC blue skies research fellowship to AY.

Ethical standards

All protocols were approved by the University of Pretoria ethics committee and complied with regulations stipulated in the Guidelines for the use of Animals in Research and complied with the current laws of the Republic of South Africa.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

265_2013_1599_MOESM1_ESM.doc (121 kb)
ESM 1 (DOC 121 kb)

References

  1. Arnold TW (2010) Uninformative parameters and model selection using Akaike’s information criterion. J Wildl Manag 74:1175–1178Google Scholar
  2. Bates D, Maechler M, Bolker B (2012) lme4: Linear mixed-effects models using S4 classes. R package version 0.999999-0, http://cran.r-project.org/web/packages/lme4/index.html. Accessed 12/02/2013
  3. Birkhead TR, Moller AP (1992) Sperm competition in birds: evolutionary causes and consequences. Academic Press, LondonGoogle Scholar
  4. Bourke AFG (1999) Colony size, social complexity and reproductive conflict in social insects. J Evol Biol 12:245–257CrossRefGoogle Scholar
  5. Cant MA (2011) The role of threats in animal cooperation. Proc R Soc Lond B 278:170–178CrossRefGoogle Scholar
  6. Cant MA, Johnstone RA (2009) How threats influence the evolutionary resolution of within-group conflict. Am Nat 173:759–771PubMedCrossRefGoogle Scholar
  7. Cant MA, Reeve HK (2002) Female control of the distribution of paternity in cooperative breeders. Am Nat 160:602–611PubMedCrossRefGoogle Scholar
  8. Cant MA, Hodge SJ, Bell MBV, Gilchrist JS, Nichols HJ (2010) Reproductive control via eviction (but not the threat of eviction) in banded mongooses. Proc R Soc Lond B 277:2219–2226CrossRefGoogle Scholar
  9. Clutton-Brock TH, Brotherton PNM, Russell AF, O’Riain MJ, Gaynor D, Kansky R, Griffin A, Manser M, Sharpe L, McIlrath GM, Small T, Moss A, Monfort S (2001) Cooperation, control, and concession in meerkat groups. Science 291:478–481PubMedCrossRefGoogle Scholar
  10. Clutton-Brock TH, Hodge SJ, Spong G, Russell AF, Jordan NR, Bennett NC, Sharpe LL, Manser MB (2006) Intrasexual competition and sexual selection in cooperative mammals. Nature 444:1065–1068PubMedCrossRefGoogle Scholar
  11. Clutton-Brock TH, Hodge SJ, Flower TP, Spong GF, Young AJ (2010) Adaptive suppression of subordinate reproduction in cooperative mammals. Am Nat 176:664–673PubMedCrossRefGoogle Scholar
  12. Collias NE, Collias EC (1978) Cooperative breeding-behavior in white-browed sparrow weaver. Auk 95:472–484Google Scholar
  13. Cooney R, Bennett NC (2000) Inbreeding avoidance and reproductive skew in a cooperative mammal. Proc R Soc Lond B 267:801–806CrossRefGoogle Scholar
  14. Cornwallis CK, West SA, Davis KE, Griffin AS (2010) Promiscuity and the evolutionary transition to complex societies. Nature 466:969–972PubMedCrossRefGoogle Scholar
  15. 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 bird. Proc R Soc Lond B 271:827–832CrossRefGoogle Scholar
  16. Creel S (2001) Social dominance and stress hormones. Trends Ecol Evol 16:491–497CrossRefGoogle Scholar
  17. Dawson DA, Horsburgh GJ, Kupper C, Stewart IRK, Ball AD, Durrant KL, Hansson B, Bacon I, Bird S, Klein A, Krupa AP, Lee JW, Martin-Galvez D, Simeoni M, Smith G, Spurgin LG, Burke T (2010) New methods to identify conserved microsatellite loci and develop primer sets of high cross-species utility—as demonstrated for birds. Mol Ecol Res 10:475–494CrossRefGoogle Scholar
  18. Double M, Cockburn A (2000) Pre-dawn infidelity: females control extra-pair mating in superb fairy-wrens. Proc R Soc Lond B 267:465–470CrossRefGoogle Scholar
  19. Emlen ST (1991) Evolution of cooperative breeding in birds and mammals. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach. Blackwell Science, Oxford, pp 301–337Google Scholar
  20. Ferguson JWH (1988) Geographic variation in social behavior of white browed sparrow weavers, Plocepasser mahali. S Afr J Zool 23:1–6Google Scholar
  21. Griffin AS, West SA (2002) Kin selection: fact and fiction. Trends Ecol Evol 17:15–21CrossRefGoogle Scholar
  22. Hamilton WD (1964) The genetical evolution of social behaviour. Parts I and II. J Theor Biol 7:1–52PubMedCrossRefGoogle Scholar
  23. Hodge SJ (2009) Understanding variation in reproductive skew: directions for future empirical research. In: Hager R, Jones CB (eds) Reproductive skew in vertebrates: proximate and ultimate causes. Cambridge University Press, Cambridge, pp 439–466CrossRefGoogle Scholar
  24. Hodge SJ, Bell MBV, Mwanguhya F, Kyabulima S, Waldick RC, Russell AF (2009) Maternal weight, offspring competitive ability, and the evolution of communal breeding. Behav Ecol 20:729–735CrossRefGoogle Scholar
  25. Holleley CE, Geerts PG (2009) Multiplex Manager 1.0: a cross-platform computer program that plans and optimizes multiplex PCR. Biotechniques 46:511–517PubMedCrossRefGoogle Scholar
  26. Johnstone RA (2000) Models of reproductive skew: a review and synthesis (invited article). Ethology 106:5–26CrossRefGoogle Scholar
  27. Johnstone RA, Cant MA (1999) Reproductive skew and the threat of eviction: a new perspective. Proc R Soc Lond B 266:275–279CrossRefGoogle Scholar
  28. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106PubMedCrossRefGoogle Scholar
  29. Keller L, Reeve HK (1994) Partitioning of reproduction in animal societies. Trends Ecol Evol 9:98–102PubMedCrossRefGoogle Scholar
  30. Kempenaers B, Dhondt AA (1993) Why do females engage in extra-pair copulations? A review of hypotheses and their predictions. Belg J Zool 123:93–103Google Scholar
  31. Koenig WD, Haydock J (2004) Incest and incest avoidance. In: Koenig WD, Dickinson JL (eds) Ecology and evolution of cooperative breeding in birds. Cambridge University Press, Cambridge, pp 142–156CrossRefGoogle Scholar
  32. Koenig WD, Haydock J, Stanback MT (1998) Reproductive roles in the cooperatively breeding acorn woodpecker: incest avoidance versus reproductive competition. Am Nat 151:243–255PubMedCrossRefGoogle Scholar
  33. Koenig WD, Shen SF, Krakauer AH, Haydock J (2009) Reproductive skew in avian societies. In: Hager R, Jones CB (eds) Reproductive skew in vertebrate societies: proximate and ultimate causes. Cambridge University Press, Cambridge, pp 227–264CrossRefGoogle Scholar
  34. Komdeur J, Kraaijeveld-Smit F, Kraaijeveld K, Edelaar P (1999) Explicit experimental evidence for the role of mate guarding in minimizing loss of paternity in the Seychelles warbler. Proc R Soc Lond B 266:2075–2081CrossRefGoogle Scholar
  35. Lewis DM (1981) Determinants of reproductive success of the white browed sparrow weaver, Plocepasser mahali. Behav Ecol Sociobiol 9:83–93CrossRefGoogle Scholar
  36. Lukas D, Clutton-Brock T (2012) Cooperative breeding and monogamy in mammalian societies. Proc R Soc Lond B 279:2151–2156CrossRefGoogle Scholar
  37. Magrath RD, Johnstone RA, Heinsohn RG (2004) Reproductive skew. In: Koenig WD, Dickinson JL (eds) Ecology and evolution of cooperative breeding in birds. Cambridge University Press, Cambridge, pp 157–176CrossRefGoogle Scholar
  38. McRae SB (1996) Family values: costs and benefits of communal nesting in the moorhen. Anim Behav 52:225–245CrossRefGoogle Scholar
  39. McRae SB, Amos W (1999) Characterization of hypervariable microsatellites in the cooperatively breeding white-browed sparrow weaver Plocepasser mahali. Mol Ecol 8:903–904PubMedGoogle Scholar
  40. McRae SB, Emlen ST, Rubenstein DR, Bogdanowicz SM (2005) Polymorphic mircosatellite loci in a plural breeder, the grey-capped social weaver (Pseudonigrita arnaudi), isolated with an improved enrichment protocol using fragment size-selection. Mol Ecol Notes 5:16–20CrossRefGoogle Scholar
  41. Mumme RL, Koenig WD, Pitelka FA (1983) Reproductive competition in the communal acorn woodpecker—sisters destroy each others eggs. Nature 306:583–584CrossRefGoogle Scholar
  42. Nelson-Flower MJ, Hockey PAR, O’Ryan C, Raihani NJ, du Plessis MJ, Ridley AR (2011) Monogamous dominant pairs monopolize reproduction in the cooperatively breeding pied babbler. Behav Ecol 22:559–565CrossRefGoogle Scholar
  43. Nicholls JA, Double MC, Rowell DM, Magrath RD (2000) The evolution of cooperative pair breeding in thornbills Acanthiza (Pardalotidae). J Avian Biol 31:165–176Google Scholar
  44. O’Riain MJ, Jarvis JUM, Alexander R, Buffenstein R, Peeters C (2000) Morphological castes in a vertebrate. Proc Natl Acad Sci USA 97:13194–13197PubMedCrossRefGoogle Scholar
  45. Peeters C, Higashi S (1989) Reproductive dominance controlled by mutilation in the queenless ant Diacamma australe. Naturwissenschaften 76:177–180CrossRefGoogle Scholar
  46. Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891CrossRefGoogle Scholar
  47. Quinn JS, Woolfenden GE, Fitzpatrick JW, White BN (1999) Multi-locus DNA fingerprinting supports genetic monogamy in Florida scrub-jays. Behav Ecol Sociobiol 45:1–10CrossRefGoogle Scholar
  48. R Development Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  49. Reeve HK, Keller L (1996) Relatedness asymmetry and reproductive sharing in animal societies. Am Nat 148:764–769CrossRefGoogle Scholar
  50. Richards SA (2008) Dealing with overdispersed count data in applied ecology. J Appl Ecol 45:218–227CrossRefGoogle Scholar
  51. 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
  52. 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 10:2263–2273Google Scholar
  53. Rousset F (2008) GENEPOP’ 007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Res 8:103–106CrossRefGoogle Scholar
  54. Rubenstein DR, Lovette IJ (2009) Reproductive skew and selection on female ornamentation in social species. Nature 462:786–789PubMedCrossRefGoogle Scholar
  55. Saltzman W, Digby LJ, Abbott DH (2009) Reproductive skew in female common marmosets: what can proximate mechanisms tell us about ultimate causes? Proc R Soc Lond B 276:389–399CrossRefGoogle Scholar
  56. Sinclair I, Ryan P (2010) Birds of Africa: South of the Sahara. Struik Publishers, JohannesburgGoogle Scholar
  57. Voigt C, Leitner S, Gahr M (2007) Socially induced brain differentiation in a cooperatively breeding songbird. Proc R Soc Lond B 274:2645–2652CrossRefGoogle Scholar
  58. Wang J (2004) Sibship reconstruction from genetic data with typing errors. Genetics 166:1963–1979PubMedCrossRefGoogle Scholar
  59. Wang JL (2011) COANCESTRY: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Mol Ecol Res 11:141–145CrossRefGoogle Scholar
  60. Wang J, Santure AW (2009) Parentage and sibship inference from multilocus genotype data under polygamy. Genetics 181:1579–1594PubMedCrossRefGoogle Scholar
  61. Wasser SK, Barash DP (1983) Reproductive suppression among female mammals—implications for biomedicine and sexual selection theory. Q Rev Biol 58:513–538PubMedCrossRefGoogle Scholar
  62. Wingfield JC, Hegner RE, Lewis DM (1991) Circulating levels of luteinizing hormone and steroid hormones in relation to social status in the cooperatively breeding white-browed sparrow weaver, Plocepasser mahali. J Zool 225:43–58CrossRefGoogle Scholar
  63. Wong MYL, Buston PM, Munday PL, Jones GP (2007) The threat of punishment enforces peaceful cooperation and stabilizes queues in a coral reef fish. Proc R Soc Lond B 274:1093–1099CrossRefGoogle Scholar
  64. York JE (2012) The evolution and regulation of dawn chorus performance in white-browed sparrow weaver society. PhD Thesis, University of BristolGoogle Scholar
  65. Young AJ (2009) The causes of physiological suppression in vertebrate societies: a synthesis. In: Hager R, Jones CB (eds) Reproductive skew in vertebrate societies: proximate and ultimate causes. Cambridge University Press, Cambridge, pp 397–437CrossRefGoogle Scholar
  66. Young AJ, Bennett NC (2010) Morphological divergence of breeders and helpers in wild Damaraland mole-rat societies. Evolution 64:3190–3197PubMedCrossRefGoogle Scholar
  67. Young AJ, Clutton-Brock TH (2006) Infanticide by subordinates influences reproductive sharing in cooperatively breeding meerkats. Biol Lett 2:385–387PubMedCrossRefGoogle Scholar
  68. Young AJ, Carlson AA, Monfort SL, Russell AF, Bennett NC, Clutton-Brock TH (2006) Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats. Proc Natl Acad Sci 103:12005–12010PubMedCrossRefGoogle Scholar
  69. Young AJ, Monfort SL, Clutton-Brock TH (2008) The causes of physiological suppression among female meerkats: a role for subordinate restraint due to the threat of infanticide? Horm Behav 53:131–139PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Xavier A. Harrison
    • 1
    • 2
  • Jennifer E. York
    • 1
  • Dominic L. Cram
    • 1
  • Michelle C. Hares
    • 1
  • Andrew J. Young
    • 1
    Email author
  1. 1.Centre for Ecology and ConservationUniversity of ExeterPenrynUK
  2. 2.Zoological Society of LondonLondonUK

Personalised recommendations