Abstract
Male-male reproductive competition occurs in many animal societies and can be costly, both through aggression or energy expenditure prior to mating and lost paternity. In most cooperative breeders, socially dominant males breed more often than do subordinates, but the costs of pre-copulatory subordinate male reproductive competition (including unsuccessful competition) have rarely been investigated in these systems. Here, we examine the association between such competition and the fitness of dominant males in the cooperatively breeding southern pied babbler (Turdoides bicolor). Babbler groups comprise a dominant breeding pair with adult subordinates of both sexes. Roughly 35 % of adult subordinate males live in groups with unrelated adult females, but despite their common engagement in active reproductive competition, these subordinate males rarely successfully breed (extra-group mating has never been detected). Overall, active reproductive competition with subordinate males is not costly to dominant males, notwithstanding that rare episodes of breeding by subordinate males cause large paternity losses (50–100 %). Specifically, the presence of an actively competing subordinate male does not affect the proportion of successful nests, the number of fledglings fathered by the dominant male or dominant male retention of dominance to the next breeding season. Instead, dominant male breeding success is likely to be more affected by factors such as food availability and group size. In the social context of cooperative breeding, a competing subordinate male may provide benefits of a larger group size or increased help; these may offset the low risk of paternity loss, possibly promoting tolerance of reproductive competitors by dominant males.
Similar content being viewed by others
References
Barton K (2014) MuMIn: multi-model inference, http://cran.r-project.org/package=MuMIn
Bates D, Maechler M, Bolker BM, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4, http://cran.r-project.org/package=lme4
Birkhead TR, Møller AP (1992) Sperm competition in birds. Academic Press, London
Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135
Bourke AFG (1988) Worker reproduction in the higher eusocial Hymenoptera. Q Rev Biol 63:291–311
Brooker MG, Rowley I, Adams M, Baverstock PR (1990) Promiscuity: an inbreeding avoidance mechanism in a socially monogamous species? Behav Ecol Sociobiol 26:191–199
Burnham KP, Anderson DR (2002) Model selection and multimodel inference, 2nd edn. Springer, New York, USA
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 277:2219–2226
Clutton-Brock TH, Albon SD, Gibson RM, Guinness FE (1979) The logical stag: adaptive aspects of fighting in red deer (Cervus elaphus L.). Anim Behav 27:211–225
Clutton-Brock TH, Brotherton PNM, Smith R, McIlrath GM, Kansky R, Gaynor D, O’Riain MJ, Skinner JD (1998) Infanticide and expulsion of females in a cooperative mammal. Proc R Soc Lond B 265:2291–2295
Cockburn A (1998) Evolution of helping behavior in cooperatively breeding birds. Annu Rev Ecol Syst 29:141–177
Cooney R, Bennett NC (2000) Inbreeding avoidance and reproductive skew in a cooperative mammal. Proc R Soc Lond B 267:801–806
Davies NB (1986) Reproductive success of dunnocks, Prunella modularis, in a variable mating system. I. Factors influencing provisioning rate, nestling weight and fledging success. J Anim Ecol 55:123–138
Díaz-Muñoz SL, DuVal EH, Krakauer AH, Lacey EA (2014) Cooperating to compete: altruism, sexual selection and causes of male reproductive cooperation. Anim Behav 88:67–78
Dierkes P, Taborsky M, Achmann R (2008) Multiple paternity in the cooperatively breeding fish Neolamprologus pulcher. Behav Ecol Sociobiol 62:1581–1589
Dierkes P, Taborsky M, Kohler U (1999) Reproductive parasitism of broodcare helpers in a cooperatively breeding fish. Behav Ecol 10:510–515
Fitzpatrick JL, Almbro M, Gonzalez-Voyer A, Kolm N, Simmons LW (2012) Male contest competition and the coevolution of weaponry and testes in pinnipeds. Evolution 66:3595–3604
Golabek KA, Radford AN (2013) Chorus-call classification in the southern pied babbler: multiple call types given in overlapping contexts. Behaviour 150:691–712
Gowaty PA (1981) An extension of the Orians-Verner-Willson model to account for mating systems besides polygyny. Am Nat 118:851–859
Griesser M, Nystrand M, Ekman J (2006) Reduced mortality selects for family cohesion in a social species. Proc R Soc Lond B 273:1881–1886
Grueber CE, Nakagawa S, Laws RJ, Jamieson IG (2011) Multimodel inference in ecology and evolution: challenges and solutions. J Evol Biol 24:699–711
Haig SM, Walters JR, Plissner JH (1994) Genetic evidence for monogamy in the cooperatively breeding red-cockaded woodpecker. Behav Ecol Sociobiol 34:295–303
Harrison XA, York JE, Cram DL, Hares MC, Young AJ (2013) Complete reproductive skew within white-browed sparrow weaver groups despite outbreeding opportunities for subordinates of both sexes. Behav Ecol Sociobiol 67:1915–1929
Haydock J, Koenig WD (2002) Reproductive skew in the polygynandrous acorn woodpecker. Proc Natl Acad Sci USA 99:7178–7183
Haydock J, Koenig WD, Stanback MT (2001) Shared parentage and incest avoidance in the cooperatively breeding acorn woodpecker. Mol Ecol 10:1515–1525
Haydock J, Parker PG, Rabenold KN (1996) Extra-pair paternity uncommon in the cooperatively breeding bicolored wren. Behav Ecol Sociobiol 38:1–16
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 439–466
Hodge SJ, Manica A, Flower T, Clutton-Brock TH (2008) Determinants of reproductive success in dominant female meerkats. J Anim Ecol 77:92–102
Hollén LI, Bell MBV, Radford AN (2008) Cooperative sentinel calling? Foragers gain increased biomass intake. Curr Biol 18:576–579
Hrdy SB (1979) Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethol Sociobiol 1:13–40
Jarvis JUM (1981) Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science 212:571–573
Kempenaers B, Verheyen GR, Dhondt AA (1997) Extrapair paternity in the blue tit (Parus caeruleus): female choice, male characteristics, and offspring quality. Behav Ecol 8:481–492
Koenig WD, Mumme RL, Stanback MT, Pitelka FA (1995) Patterns and consequences of egg destruction among joint-nesting acorn woodpeckers. Anim Behav 50:607–621
Koenig WD, Shen S, Krakauer AH, Haydock J (2009) Reproductive skew in avian societies. In: Hager R, Jones CB (eds) Reproductive skew in vertebrates: proximate and ultimate causes. Cambridge University Press, Cambridge, pp 227–264
Kokko H, Ekman J (2002) Delayed dispersal as a route to breeding: territorial inheritance, safe havens, and ecological constraints. Am Nat 160:468–484
Lardy S, Cohas A, Desouhant E, Tafani M, Allainé D (2012) Paternity and dominance loss in male breeders: the cost of helpers in a cooperatively breeding mammal. PLoS One 7, e29508
Le Boeuf BJ (1974) Male-male competition and reproductive success in elephant seals. Am Zool 14:163–176
Legge S, Cockburn A (2000) Social and mating system of cooperatively breeding laughing kookaburras (Dacelo novaeguineae). Behav Ecol Sociobiol 47:220–229
Li S-H, Brown JL (2002) Reduction of maternal care: a new benefit of multiple mating? Behav Ecol 13:87–93
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
Mulder RA, Dunn PO, Cockburn A, Lazenby-Cohen KA, Howell MJ (1994) Helpers liberate female fairy-wrens from constraints on extra-pair mate choice. Proc R Soc Lond B 255:223–229
Mumme RL, Koenig WD, Pitelka FA (1983) Mate guarding in the acorn woodpecker: within-group reproductive competition in a cooperative breeder. Anim Behav 31:1094–1106
Nelson-Flower MJ (2010) Kinship and its consequences in the cooperatively breeding Southern Pied Babbler Turdoides bicolor. University of Cape Town, PhD dissertation
Nelson-Flower MJ, Hockey PAR, O’Ryan C, English S, Thompson AM, Bradley K, Rose R, Ridley AR (2013) Costly reproductive competition between females in a monogamous cooperatively breeding bird. Proc R Soc B 280:20130728
Nelson-Flower MJ, Hockey PAR, O’Ryan C, Raihani NJ, du Plessis MA, Ridley AR (2011) Monogamous dominant pairs monopolize reproduction in the cooperatively breeding pied babbler. Behav Ecol 22:559–565
Nelson-Flower MJ, Hockey PAR, O’Ryan C, Ridley AR (2012) Inbreeding avoidance mechanisms: dispersal dynamics in cooperatively breeding southern pied babblers. J Anim Ecol 81:876–883
O’Riain MJ, Bennett NC, Brotherton PNM, McIlrath GM, Clutton-Brock TH (2000) Reproductive suppression and inbreeding avoidance in wild populations of co-operatively breeding meerkats (Suricata suricatta). Behav Ecol Sociobiol 48:471–477
Parker GA, Lessells CM, Simmons LW (2012) Sperm competition games: a general model for precopulatory male–male competition. Evolution 67:95–109
Piper WH, Slater G (1993) Polyandry and incest avoidance in the cooperative stripe-backed wren of Venezuela. Behaviour 124:227–247
Pitcher TE, Doucet SM, Beausoleil J-MJ, Hanley D (2009) Secondary sexual characters and sperm traits in coho salmon Oncorhynchus kisutch. J Fish Biol 74:1450–1461
Preston BT, Saint Jalme M, Hingrat Y, Lacroix F, Sorci G (2011) Sexually extravagant males age more rapidly. Ecol Lett 14:1017–1024
R Core Team (2014) R: a language and environment for statistical computing, http://www.r-project.org
Rabenold PP, Rabenold KN, Piper WH, Haydock J, Zack SW (1990) Shared paternity revealed by genetic analysis in cooperatively breeding tropical wrens. Nature 348:538–540
Radford AN, Ridley AR (2007) Individuals in foraging groups may use vocal cues when assessing their need for anti-predator vigilance. Biol Lett 3:249–252
Raihani NJ, Nelson-Flower MJ, Golabek KA, Ridley AR (2010) Routes to breeding in cooperatively breeding pied babblers Turdoides bicolor. J Avian Biol 41:681–686
Raihani NJ, Ridley AR (2007) Variable fledging age according to group size: trade-offs in a cooperatively breeding bird. Biol Lett 3:624–627
Ridley AR, Raihani NJ (2007) Variable postfledging care in a cooperative bird: causes and consequences. Behav Ecol 18:994–1000
Ridley AR, Raihani NJ (2008) Task partitioning increases reproductive output in a cooperative bird. Behav Ecol 19:1136–1142
Ridley AR, Raihani NJ, Nelson-Flower MJ (2008) The cost of being alone: the fate of floaters in a population of cooperatively breeding pied babblers Turdoides bicolor. J Avian Biol 39:389–392
Rubenstein DR (2007) Female extrapair mate choice in a cooperative breeder: trading sex for help and increasing offspring heterozygosity. Proc R Soc Lond B 274:1895–1903
Spong GF, Hodge SJ, Young AJ, Clutton-Brock TH (2008) Factors affecting the reproductive success of dominant male meerkats. Mol Ecol 17:2287–2299
Townsend AK, Bowman R, Fitzpatrick JW, Dent M, Lovette IJ (2011) Genetic monogamy across variable demographic landscapes in cooperatively breeding Florida scrub-jays. Behav Ecol 22:464–470
Townsend AK, Clark AB, McGowan KJ (2010) Direct benefits and genetic costs of extrapair paternity for female American crows (Corvus brachyrhynchos). Am Nat 175:E1–E9
Trail PW (1985) Courtship disruption modifies mate choice in a lek-breeding bird. Science 227:778–780
Van den Berghe EP (1988) Piracy as an alternative reproductive tactic for males. Nature 334:697–698
Van den Berghe EP, Wernerus F, Warner RR (1989) Female choice and the mating cost of peripheral males. Anim Behav 38:875–884
Warrington MH, Rollins LA, Raihani NJ, Russell AF, Griffith SC (2013) Genetic monogamy despite variable ecological conditions and social environment in the cooperatively breeding apostlebird. Ecol Evol 3:4669–4682
Acknowledgments
We thank T. Clutton-Brock and the staff at the Kuruman River Reserve for support for the Pied Babbler Research Project. The Kotzes and the de Bruins allowed land access. M. Bell, K. Bradley, S. Engesser, F. Finch, T.P. Flower, K. Golabek, D. Humphries, A. Radford, N. Raihani, R. Rose, A. Thompson, J. Westrip, E. Wiley and assistants helped with collecting data and maintaining habituation of babbler groups. Statistical help was provided by S. English, R. Mares and A. W. Bateman. Helpful discussion and comments were provided by S. English, T. P. Flower and R. Mares, and two anonymous reviewers. Grateful thanks to T.P. Flower for logistical support. Financial support was provided by the DST-NRF Centre of Excellence at the Percy FitzPatrick Institute for African Ornithology at the University of Cape Town to MJN-F and ARR and by the National Science and Engineering Council of Canada to MJNF.
Compliance with ethical standards
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 University of Cape Town. The Northern Cape Conservation Authority permitted research on pied babblers, and fieldwork received ethical clearance from the University of Cape Town’s Animal Ethics Committee (AEC no. 2006/V15/AR).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by D. Rubenstein
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 29 kb)
Rights and permissions
About this article
Cite this article
Nelson-Flower, M.J., Ridley, A.R. Male-male competition is not costly to dominant males in a cooperatively breeding bird. Behav Ecol Sociobiol 69, 1997–2004 (2015). https://doi.org/10.1007/s00265-015-2011-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-015-2011-0