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Article << Previous     |     Next >>   Contents Vol 113(3)

Evolutionary origins and persistence of infidelity in Malurus: the least faithful birds

Andrew Cockburn A B , Lyanne Brouwer A , Michael C. Double A , Nicolas Margraf A and Martijn van de Pol A

A Evolution, Ecology and Genetics, Research School of Biology, The Australian National University, Canberra, ACT 0200, Australia.
B Corresponding author. Email: andrew.cockburn@anu.edu.au

Emu 113(3) 208-217 http://dx.doi.org/10.1071/MU12094
Submitted: 14 October 2012  Accepted: 29 November 2012   Published: 15 August 2013


 
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Abstract

Fairy-wrens (genus Malurus) maintain territories year round, and breed cooperatively, with all members of the social group provisioning young. Despite living with several adult males, the breeding female typically cuckolds all of them, seeking fertilisations from extra-group males that provide no care to her offspring, instead caring for the young reared on their own territory. We trace the evolutionary origins and persistence of this extraordinary combination of traits. We argue that the high rate of infidelity in some fairy-wrens facilitates social pairing among nuclear family relatives, rather than being an evolutionary response to avoid inbreeding. It seems likely that females mate with extra-group males to improve the genetic quality of their offspring. The ability of males to maintain breeding plumage for long periods is the primary criterion for female choice; only older males can do so. Several features of the mating system undermine the accuracy of female choice, and low-quality males exploit this uncertainty. Extra-group matings by low-quality males can help stabilise the mating system but may leave it vulnerable to collapse under certain circumstances. Nonetheless, sexual selection in most species is very strong, confirming the utility of fairy-wrens as model organisms for the study of mate choice and intersexual selection.

Additional keywords: cooperative breeding, extra-pair copulation, fairy-wren, Maluridae, sperm competition.


References

Birkhead, T. R., and Møller, A. P. (1992). ‘Sperm Competition in Birds: Evolutionary Causes and Consequences.’ (Academic Press: London.)

Bitton, P.-P., O’Brien, E. L., and Dawson, R. D. (2007). Plumage brightness and age predict extrapair fertilization success of male Tree Swallows, Tachycineta bicolor. Animal Behaviour 74, 1777–1784.
CrossRef |

Bouwman, K. M., and Komdeur, J. (2005). Old female Reed Buntings (Emberiza schoeniclus) increase extra-pair paternity in their broods when mated to young males. Behaviour 142, 1449–1463.
CrossRef |

Bouwman, K. M., Burke, T., and Komdeur, J. (2006). How female Reed Buntings benefit from extra-pair mating behaviour: testing hypotheses through patterns of paternity in sequential broods. Molecular Ecology 15, 2589–2600.
CrossRef | CAS | PubMed |

Bouwman, K. M., Van Dijk, R. E., Wijmenga, J. J., and Komdeur, J. (2007). Older male Reed Buntings are more successful at gaining extrapair fertilizations. Animal Behaviour 73, 15–27.
CrossRef |

Brooker, M. G., Rowley, I., Adams, M., and Baverstock, P. R. (1990). Promiscuity: an inbreeding avoidance mechanism in a socially monogamous species? Behavioral Ecology and Sociobiology 26, 191–200.

Brouwer, L., van de Pol, M., Atema, E., and Cockburn, A. (2011). Strategic promiscuity helps avoid inbreeding at multiple levels in a cooperative breeder where both sexes are philopatric. Molecular Ecology 20, 4796–4807.
CrossRef | PubMed |

Calhim, S., Double, M. C., Margraf, N., Birkhead, T. R., and Cockburn, A. (2011). Maintenance of sperm variation in a highly promiscuous wild bird. PLoS ONE 6, e28809.
CrossRef | CAS | PubMed |

Carrick, R. (1963). Ecological significance of territory in the Australian Magpie, Gymnorhina tibicen. Proceedings of the International Ornithological Congress 13, 740–753.
CrossRef |

Carrick, R. (1972). Population ecology of the Australian black-backed magpie, Royal Penguin and Silver Gull. US Department of the Interior Internal Wildlife Reports 2, 41–99.

Coates, B. J. (1990). ‘The Birds of Papua New Guinea. Vol. 2: Passerines.’ (Dove Publications: Alderley, Qld.)

Cockburn, A. (2004). Mating systems and sexual conflict. In ‘Ecology and Evolution of Cooperative Breeding in Birds.’ (Eds W. D. Koenig and J. L. Dickinson.) pp. 81–101. (Cambridge University Press: Cambridge, UK.)

Cockburn, A. (2006). Prevalence of different modes of parental care in birds. Proceedings of the Royal Society of London – B. Biological Sciences 273, 1375–1383.
CrossRef |

Cockburn, A. (2013). Cooperative breeding in birds: towards a richer conceptual framework. In ‘Cooperation and its Evolution.’ (Eds K. Sterelny, R. Joyce, B. Calcott and B. Fraser.) pp. 223–245. (MIT Press: Cambridge, MA.)

Cockburn, A., Osmond, H. L., Mulder, R. A., Green, D. J., and Double, M. C. (2003). Divorce, dispersal and incest avoidance in the cooperatively breeding Superb Fairy-wren Malurus cyaneus. Journal of Animal Ecology 72, 189–202.
CrossRef |

Cockburn, A., Osmond, H. L., and Double, M. C. (2008a). Swingin’ in the rain: condition dependence and sexual selection in a capricious world. Proceedings of the Royal Society of London – B. Biological Sciences 275, 605–612.
CrossRef |

Cockburn, A., Osmond, H. L., Mulder, R. A., Double, M. C., and Green, D. J. (2008b). Demography of male reproductive queues in cooperatively breeding Superb Fairy-wrens Malurus cyaneus. Journal of Animal Ecology 77, 297–304.
CrossRef | PubMed |

Cockburn, A., Sims, R. A., Osmond, H. L., Green, D. J., Double, M. C., and Mulder, R. A. (2008c). Can we measure the benefits of help in cooperatively breeding birds: the case of Superb Fairy-wrens Malurus cyaneus? Journal of Animal Ecology 77, 430–438.
CrossRef | PubMed |

Cockburn, A., Dalziell, A. H., Blackmore, C. J., Double, M. C., Kokko, H., Osmond, H. L., Beck, N. R., Head, M. L., and Wells, K. (2009). Superb Fairy-wren males aggregate into hidden leks to solicit extragroup fertilizations before dawn. Behavioral Ecology 20, 501–510.
CrossRef |

Colombelli-Négrel, D., Schlotfeldt, B. E., and Kleindorfer, S. (2009). High levels of extra-pair paternity in Superb Fairy-wrens in South Australia despite low frequency of auxiliary males. Emu 109, 300–304.
CrossRef |

Dalziell, A. H., and Cockburn, A. (2008). Dawn song in Superb Fairy-wrens: a bird that seeks extrapair copulations during the dawn chorus. Animal Behaviour 75, 489–500.
CrossRef |

Dixon, A., Ross, D., O’Malley, S. L. C., and Burke, T. (1994). Paternal investment inversely related to degree of extra-pair paternity in the Reed Bunting. Nature 371, 698–700.
CrossRef |

Double, M., and Cockburn, A. (2000). Pre-dawn infidelity: females control extra-pair mating in Superb Fairy-wrens. Proceedings of the Royal Society of London – B. Biological Sciences 267, 465–470.
CrossRef | CAS |

Double, M. C., and Cockburn, A. (2003). Subordinate Superb Fairy-wrens (Malurus cyaneus) parasitize the reproductive success of attractive dominant males. Proceedings of the Royal Society of London – B. Biological Sciences 270, 379–384.
CrossRef |

Double, M. C., Peakall, R., Beck, N. R., and Cockburn, A. (2005). Dispersal, philopatry, and infidelity: dissecting local genetic structure in Superb Fairy-wrens (Malurus cyaneus). Evolution 59, 625–635.
| CAS | PubMed |

Driskell, A. C., Norman, J. A., Pruett-Jones, S., Mangall, E., Sonsthagen, S., and Christidis, L. (2011). A multigene phylogeny examining evolutionary and ecological relationships in the Australo-papuan wrens of the subfamily Malurinae (Aves). Molecular Phylogenetics and Evolution 60, 480–485.
CrossRef | PubMed |

Dunn, P. O., and Cockburn, A. (1999). Extrapair mate choice and honest signaling in cooperatively breeding Superb Fairy-wrens. Evolution 53, 938–946.
CrossRef |

Dunn, P. O., Cockburn, A., and Mulder, R. A. (1995). Fairy-wren helpers often care for young to which they are unrelated. Proceedings of the Royal Society of London – B. Biological Sciences 259, 339–343.
CrossRef |

Dunn, P. O., Lifjeld, J. T., and Whittingham, L. A. (2009). Multiple paternity and offspring quality in Tree Swallows. Behavioral Ecology and Sociobiology 63, 911–922.
CrossRef |

Durrant, K. L., and Hughes, J. M. (2005). Differing rates of extra-group paternity between two populations of the Australian Magpie (Gymnorhina tibicen). Behavioral Ecology and Sociobiology 57, 536–545.
CrossRef |

Durrant, K. L., and Hughes, J. M. (2006). Are there correlates of male Australian Magpie Gymnorhina tibicen reproductive success in a population with high rates of extra-group paternity? Ibis 148, 313–320.
CrossRef |

Finn, P. G., and Hughes, J. M. (2001). Helping behaviour in Australian Magpies, Gymnorhina tibicen. Emu 101, 57–63.
CrossRef |

Friedman, N. R., Hofmann, C. M., Kondo, B., and Omland, K. E. (2009). Correlated evolution of migration and sexual dichromatism in the New World orioles (Icterus). Evolution 63, 3269–3274.
CrossRef | PubMed |

Gardner, J. L., Trueman, J. W. H., Ebert, D., Joseph, L., and Magrath, R. D. (2010). Phylogeny and evolution of the Meliphagoidea, the largest radiation of Australasian songbirds. Molecular Phylogenetics and Evolution 55, 1087–1102.
CrossRef | PubMed |

Gowaty, P. A. (1996). Battle of the sexes and the origins of monogamy. In ‘Partnerships in Birds: The Study of Monogamy.’ (Ed. J. M. Black.) pp. 21–52. (Oxford University Press: Oxford, UK.)

Green, D. J., Cockburn, A., Hall, M. L., Osmond, H., and Dunn, P. O. (1995). Increased opportunities for cuckoldry may be why dominant male fairy-wrens tolerate helpers. Proceedings of the Royal Society of London – B. Biological Sciences 262, 297–303.
CrossRef |

Green, D. J., Osmond, H. L., Double, M. C., and Cockburn, A. (2000). Display rate by male fairy-wrens (Malurus cyaneus) during the fertile period of females has little influence on extra-pair mate choice. Behavioral Ecology and Sociobiology 48, 438–446.
CrossRef |

Greig, E. I., and Pruett-Jones, S. (2009). A predator-elicited song in the Splendid Fairy-wren: warning signal or intraspecific display? Animal Behaviour 78, 45–52.
CrossRef |

Greig, E. I., Spendel, K., and Brandley, N. C. (2010). A predator-elicited vocalisation in the Variegated Fairy-wren (Malurus lamberti). Emu 110, 165–169.
CrossRef |

Griffith, S. C., Owens, I. P. F., and Thuman, K. A. (2002). Extra pair paternity in birds: a review of interspecific variation and adaptive function. Molecular Ecology 11, 2195–2212.
CrossRef | CAS | PubMed |

Hughes, J. M., Mather, P. B., Toon, A., Ma, J., Rowley, I., and Russell, E. (2003). High levels of extra-group paternity in a population of Australian Magpies Gymnorhina tibicen: evidence from microsatellite analysis. Molecular Ecology 12, 3441–3450.
CrossRef | CAS | PubMed |

Joseph, L., Edwards, S. V., and McLean, A. J. (2013). The Maluridae: inferring avian biology and evolutionary history from DNA sequences. Emu 113, 195–207.
CrossRef |

Karubian, J. (2001). The social organization and mating system of the Striated Grasswren. Condor 103, 412–417.
CrossRef |

Karubian, J. (2002). Costs and benefits of variable breeding plumage in the Red-backed Fairy-wren. Evolution 56, 1673–1682.
| PubMed |

Karubian, J., and Alvarado, A. (2003). Testing the function of petal-carrying in the Red-backed Fairy-wren (Malurus melanocephalus). Emu 103, 87–92.
CrossRef |

Kempenaers, B., Congdon, B., Boag, P., and Robertson, R. J. (1999). Extrapair paternity and egg hatchability in Tree Swallows: evidence for the genetic compatibility hypothesis? Behavioral Ecology 10, 304–311.
CrossRef |

Kingma, S. A., Hall, M. L., Segelbacher, G., and Peters, A. (2009). Radical loss of an extreme extra-pair mating system. BMC Ecology 9, 15.
CrossRef | PubMed |

Kleven, O., and Lifjeld, J. T. (2004). Extrapair paternity and offspring immunocompetence in the Reed Bunting, Emberiza schoeniclus. Animal Behaviour 68, 283–289.
CrossRef |

Kleven, O., and Lifjeld, J. T. (2005). No evidence for increased offspring heterozygosity from extrapair mating in the Reed Bunting (Emberiza schoeniclus). Behavioral Ecology 16, 561–565.
CrossRef |

Kruuk, L. E. B. (2004). Estimating genetic parameters in natural populations using the ‘animal model’. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 359, 873–890.
CrossRef |

Lack, D. (1947). The significance of clutch size. Ibis 89, 302–352.
CrossRef |

Langmore, N. E., and Mulder, R. A. (1992). A novel context for bird song: predator calls prompt male singing in the kleptogamous Superb Fairy-wren, Malurus cyaneus. Ethology 90, 143–153.
CrossRef |

Lee, J. Y., Joseph, L., and Edwards, S. V. (2012). A species tree for the Australo-Papuan fairy-wrens and allies (Aves : Maluridae). Systematic Biology 61, 253–271.
CrossRef | CAS | PubMed |

Maguire, G. S., and Mulder, R. A. (2008). Low levels of extra-pair paternity in Southern Emu-wrens (Aves : Maluridae). Australian Journal of Zoology 56, 79–84.
CrossRef |

McFarlane, M. L., Cherry, M. I., and Evans, M. R. (2010a). Female Cape Sugarbirds (Promerops cafer) modify egg investment both for extra-pair mates and for male tail length. Journal of Evolutionary Biology 23, 1998–2003.
CrossRef | CAS | PubMed |

McFarlane, M. L., Evans, M. R., Feldheim, K. A., Preault, M., Bowie, R. C. K., and Cherry, M. I. (2010b). Long tails matter in sugarbirds: positively for extra-pair but negatively for within-pair fertilization success. Behavioral Ecology 21, 26–32.
CrossRef |

Møller, A. P. (1992). Frequency of female copulations with multiple males and sexual selection. American Naturalist 139, 1089–1101.
CrossRef |

Mulder, R. A. (1997). Extra-group courtship displays and other reproductive tactics of Superb Fairy-wrens. Australian Journal of Zoology 45, 131–143.
CrossRef |

Mulder, R. A., and Langmore, N. E. (1993). Dominant males punish helpers for temporary defection in Superb Fairy-wrens. Animal Behaviour 45, 830–833.
CrossRef |

Mulder, R. A., Dunn, P. O., Cockburn, A., Lazenby-Cohen, K. A., and Howell, M. J. (1994). Helpers liberate female fairy-wrens from constraints on extra-pair mate choice. Proceedings of the Royal Society of London – B. Biological Sciences 255, 223–229.
CrossRef |

Perrins, C. M. (1965). Population fluctuation and clutch-size in the Great Tit, Parus major L. Journal of Animal Ecology 34, 601–647.
CrossRef |

Peters, A. (2000). Testosterone treatment is immunosuppressive in Superb Fairy-wrens, yet free-living males with high testosterone are more immunocompetent. Proceedings of the Royal Society of London – B. Biological Sciences 267, 883–889.
CrossRef | CAS |

Peters, A., Astheimer, L. B., Boland, C. R. J., and Cockburn, A. (2000). Testosterone is involved in acquisition and maintenance of sexually selected male plumage in Superb Fairy-wrens, Malurus cyaneus. Behavioral Ecology and Sociobiology 47, 438–445.
CrossRef |

Peters, A., Astheimer, L. B., and Cockburn, A. (2001). The annual testosterone profile in cooperatively breeding Superb Fairy-wrens, Malurus cyaneus, reflects their extreme infidelity. Behavioral Ecology and Sociobiology 50, 519–527.
CrossRef |

Rowe, M., and Pruett-Jones, S. (2008). Reproductive anatomy of male Southern Emu-wrens (Stipiturus malachurus) and Striated Grasswrens (Amytornis striatus). Emu 108, 68–73.
CrossRef |

Rowley, I. (1991). Petal-carrying by fairy-wrens of the genus Malurus. Australian Bird Watcher 14, 75–81.

Rowley, I., and Russell, E. (1990). Philandering: a mixed mating strategy in the Splendid Fairy-wren Malurus splendens. Behavioral Ecology and Sociobiology 27, 431–437.
CrossRef |

Rowley, I., and Russell, E. (1997). ‘Fairy-wrens and Grasswrens: Maluridae.’ (Oxford University Press: Oxford, UK.)

Rowley, I., Russell, E., and Brooker, M. (1986). Inbreeding: benefits may outweigh costs. Animal Behaviour 34, 939–941.
CrossRef |

Rubenstein, D. R. (2012). Family feuds: social competition and sexual conflict in complex societies. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 367, 2304–2313.
CrossRef |

Russell, E. M., and Rowley, I. (1993). Demography of the cooperatively breeding Splendid Fairy-wren, Malurus splendens (Maluridae). Australian Journal of Zoology 41, 475–505.
CrossRef |

Russell, E., and Rowley, I. (2000). Demography and social organisation of the Red-winged Fairy-wren, Malurus elegans. Australian Journal of Zoology 48, 161–200.
CrossRef |

Russell, A. F., Langmore, N. E., Cockburn, A., Astheimer, L. B., and Kilner, R. M. (2007). Reduced egg investment can conceal helper effects in cooperatively breeding birds. Science 317, 941–944.
CrossRef | CAS | PubMed |

Schmoll, T. (2011). A review and perspective on context-dependent genetic effects of extra-pair mating in birds. Journal of Ornithology 152, 265–277.
CrossRef |

Schodde, R., and Weatherly, R. (1982). ‘The Fairy-wrens: a Monograph of the Maluridae.’ (Lansdowne: Melbourne.)

Sheldon, B. C. (2000). Differential allocation: tests, mechanisms and implications. Trends in Ecology & Evolution 15, 397–402.
CrossRef |

Stapleton, M. K., Kleven, O., Lifjeld, J. T., and Robertson, R. J. (2007). Female Tree Swallows (Tachycineta bicolor) increase offspring heterozygosity through extrapair mating. Behavioral Ecology and Sociobiology 61, 1725–1733.
CrossRef |

Strong, M. (1990). Furgling by the Red-backed Fairy-wren. Sunbird 20, 37–38.

Suter, S. M., Keiser, M., Feignoux, R., and Meyer, D. R. (2007). Reed Bunting females increase fitness through extra-pair mating with genetically dissimilar males. Proceedings of the Royal Society of London – B. Biological Sciences 274, 2865–2871.
CrossRef |

Suter, S. M., Bielanska, J., Roethlin-Spillmann, S., Strambini, L., and Meyer, D. R. (2009). The cost of infidelity to female Reed Buntings. Behavioral Ecology 20, 601–608.
CrossRef |

Tarvin, K. A., Webster, M. S., Tuttle, E. M., and Pruett-Jones, S. (2005). Genetic similarity of social mates predicts the level of extrapair paternity in Splendid Fairy-wrens. Animal Behaviour 70, 945–955.
CrossRef |

Tschirren, B., Postma, E., Rutstein, A. N., and Griffith, S. C. (2012). When mothers make sons sexy: maternal effects contribute to the increased sexual attractiveness of extra-pair offspring. Proceedings of the Royal Society of London – B. Biological Sciences 279, 1233–1240.
CrossRef |

Tuttle, E. M., and Pruett-Jones, S. (2004). Estimates of extreme sperm production: morphological and experimental evidence from reproductively promiscuous fairy-wrens (Malurus). Animal Behaviour 68, 541–550.
CrossRef |

Tuttle, E. M., and Pruett-Jones, S. (2007). Erratum. Animal Behaviour 73, 555–556.
CrossRef |

van de Pol, M., and Cockburn, A. (2011). Identifying the critical climatic time window that affects trait expression. American Naturalist 177, 698–707.
CrossRef | PubMed |

van de Pol, M., Osmond, H. L., and Cockburn, A. (2012). Fluctuations in population composition dampen the impact of phenotypic plasticity on trait dynamics in Superb Fairy-wrens. Journal of Animal Ecology 81, 411–422.
CrossRef | PubMed |

Varian-Ramos, C. W., and Webster, M. S. (2012). Extrapair copulations reduce inbreeding for female Red-backed Fairy-wrens, Malurus melanocephalus. Animal Behaviour 83, 857–864.
CrossRef |

Webster, M. S., Tarvin, K. A., Tuttle, E. M., and Pruett-Jones, S. (2004). Reproductive promiscuity in the Splendid Fairy-wren: effects of group size and auxiliary reproduction. Behavioral Ecology 15, 907–915.
CrossRef |

Webster, M. S., Tarvin, K. A., Tuttle, E. M., and Pruett-Jones, S. (2007). Promiscuity drives sexual selection in a socially monogamous bird. Evolution 61, 2205–2211.
CrossRef | PubMed |

Webster, M. S., Varian-Ramos, C. W., and Karubian, J. (2008). Plumage color and reproduction in the Red-backed Fairy-wren: why be a dull breeder? Behavioral Ecology 19, 517–524.
CrossRef |

Westneat, D. F., and Stewart, I. R. K. (2003). Extra-pair paternity in birds: causes, correlates, and conflict. Annual Review of Ecology Evolution and Systematics 34, 365–396.
CrossRef |

Whittingham, L. A., Dunn, P. O., and Stapleton, M. K. (2006). Repeatability of extra-pair mating in Tree Swallows. Molecular Ecology 15, 841–849.
CrossRef | PubMed |


   
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