Breaking the rules: sex roles and genetic mating system of the pheasant coucal

Abstract

Generally in birds, the classic sex roles of male competition and female choice result in females providing most offspring care while males face uncertain parentage. In less than 5% of species, however, reversed courtship sex roles lead to predominantly male care and low extra-pair paternity. These role-reversed species usually have reversed sexual size dimorphism and polyandry, confirming that sexual selection acts most strongly on the sex with the smaller parental investment and accordingly higher potential reproductive rate. We used parentage analyses and observations from three field seasons to establish the social and genetic mating system of pheasant coucals, Centropus phasianinus, a tropical nesting cuckoo, where males are much smaller than females and provide most parental care. Pheasant coucals are socially monogamous and in this study males produced about 80% of calls in the dawn chorus, implying greater male sexual competition. Despite the substantial male investments, extra-pair paternity was unusually high for a socially monogamous, duetting species. Using two or more mismatches to determine extra-pair parentage, we found that 11 of 59 young (18.6%) in 10 of 21 broods (47.6%) were not sired by their putative father. Male incubation, starting early in the laying sequence, may give the female opportunity and reason to seek these extra-pair copulations. Monogamy, rather than the polyandry and sex-role reversal typical of its congener, C. grillii, may be the result of the large territory size, which could prevent females from monopolising multiple males. The pheasant coucal’s exceptional combination of classic sex-roles and male-biased care for extra-pair young is hard to reconcile with current sexual selection theory, but may represent an intermediate stage in the evolution of polyandry or an evolutionary remnant of polyandry.

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References

  1. Andersson M (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  2. Andersson M (1995) Evolution of reversed sex roles, sexual size dimorphism, and mating system in coucals (Centropodidae, Aves). Biol J Linn Soc 54:173–181

    Article  Google Scholar 

  3. Andersson M (2005) Evolution of classical polyandry: three steps to female emancipation. Ethology 111:1–23

    Article  Google Scholar 

  4. Andersson M, Norberg RA (1981) Evolution of reversed sexual size dimorphism and role partitioning among predatory birds, with a size scaling of flight performance. Biol J Linn Soc 15:105–130

    Article  Google Scholar 

  5. Birkhead TR, Møller AP (1992) Sperm competition in birds: evolutionary causes and consequences. Academic, London

    Google Scholar 

  6. Blanckenhorn WU (2005) Behavioral causes and consequences of sexual size dimorphism. Ethology 111:977–1016

    Article  Google Scholar 

  7. Brohede J, Primmer CR, Møller A, Ellegren H (2002) Heterogeneity in the rate and pattern of germline mutation at individual microsatellite loci. Nucleic Acids Res 30:1997–2003

    PubMed  Article  CAS  Google Scholar 

  8. Butchart SHM, Seddon N, Ekstrom JMM (1999) Polyandry and competition for territories in bronze-winged jacanas. J Anim Ecol 68:928–939

    Article  Google Scholar 

  9. Calder WAI (1967) Breeding behavior of the roadrunner, Geococcyx californianus. Auk 84:597–598

    Google Scholar 

  10. Carlson A (1989) Courtship feeding and clutch size in red-backed shrikes (Lanius collurio). Am Nat 133:454–457

    Article  Google Scholar 

  11. Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton

    Google Scholar 

  12. Clutton-Brock TH, Parker GA (1992) Potential reproductive rates and the operation of sexual selection. Q Rev Biol 67:437–456

    Article  Google Scholar 

  13. Clutton-Brock TH, Vincent ACJ (1991) Sexual selection and the potential reproductive rates of males and females. Nature 351:58–60

    PubMed  Article  CAS  Google Scholar 

  14. Cockburn A (2006) Prevalence of different modes of parental care in birds. Proc Biol Sci 273:1375–1383

    PubMed  Article  Google Scholar 

  15. Colwell MA, Oring LW (1989) Extra-pair mating in the spotted sandpiper: a female mate acquisition tactic. Anim Behav 38:675–684

    Article  Google Scholar 

  16. Darwin C (1871) The descent of man and selection in relation to sex. John Murray, London

    Google Scholar 

  17. Dawkins R, Carlisle TR (1976) Parental investment, mate desertion and a fallacy. Nature 262:131–133

    Article  Google Scholar 

  18. Delehanty DJ, Fleischer RC, Colwell MA, Oring LW (1998) Sex-role reversal and the absence of extra-pair fertilization in Wilson’s phalaropes. Anim Behav 55:995–1002

    PubMed  Article  Google Scholar 

  19. Emlen ST, Wrege PH (2004) Size dimorphism, intrasexual competition, and sexual selection in wattled jacana (Jacana jacana), a sex-role-reversed shorebird in Panama. Auk 121:391–403

    Article  Google Scholar 

  20. Geberzahn N, Goymann W, Muck C, ten Cate C (2009) Females alter their song when challenged in a sex-role reversed bird species. Behav Ecol Sociobiol 64:193–204

    PubMed  Article  Google Scholar 

  21. Gill SA, Vonhof MJ, Stutchbury BJ, Morton ES, Quinn JS (2005) No evidence for acoustic mate-guarding in duetting buff-breasted wrens (Thryothorus leucotis). Behav Ecol Sociobiol 57:557–565

    Article  Google Scholar 

  22. Goymann W, Wingfield JC (2004) Competing females and caring males. Sex steroids in African black coucals, Centropus grillii. Anim Behav 68:733–740

    Article  Google Scholar 

  23. Goymann W, Wittenzellner A, Wingfield J (2004) Competing females and caring males. Polyandry and sex-role reversal in African black coucals, Centropus grillii. Ethology 110:807–823

    Article  Google Scholar 

  24. Goymann W, Kempenaers B, Wingfield J (2005) Breeding biology, sexually dimorphic development and nestling testosterone concentrations of the classically polyandrous African black coucal, Centropus grillii. J Ornithol 146:314–324

    Article  Google Scholar 

  25. 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

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  27. Hall ML (2004) A review of hypotheses for the functions of avian duetting. Behav Ecol Sociobiol 55:415–430

    Article  Google Scholar 

  28. Hall ML (2009) A review of vocal duetting in birds. Adv Stud Behav 40:67–121

    Article  Google Scholar 

  29. Hall ML, Magrath RD (2000) Duetting and mate-guarding in Australian magpie-larks (Grallina cyanoleuca). Behav Ecol Sociobiol 47:180–187

    Article  Google Scholar 

  30. Heinsohn R, Legge S, Endler JA (2005) Extreme reversed sexual dichromatism in a bird without sex role reversal. Science 309:617–619

    PubMed  Article  CAS  Google Scholar 

  31. Hicks RK, Restall R (1992) Pheasant coucal Centropus phasianinus attacking birds caught in a mist net. Muruk 5:143

    Google Scholar 

  32. Higgins PJ (1999) Handbook of Australian, New Zealand and Antarctic birds. Volume 4: parrots to Dollarbirds. Oxford University Press, Melbourne

    Google Scholar 

  33. Jenni DA (1974) Evolution of polyandry in birds. Am Zool 14:129–144

    Google Scholar 

  34. Jones RC, Lin M (1993) Spermatogenesis in birds. Oxf Rev Reprod Biol 15:234–264

    Google Scholar 

  35. Klump GM (1996) Bird communication in a noisy world. In: Kroodsma DE, Miller EH (eds) Ecology and evolution of acoustic communication in birds. Cornell University press, Ithaca, pp 321–338

    Google Scholar 

  36. Kokko H, Jennions M (2008) Parental investment, sexual selection and sex ratios. J Evol Biol 21:919–948

    PubMed  Article  Google Scholar 

  37. Lack D (1968) Ecological adaptations for breeding in birds. Methuen, London

    Google Scholar 

  38. Langmore NE (1998) Functions of duet and solo songs of female birds. Trends Ecol Evol 13:136–140

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  40. Maurer G (2007a) Ecology and evolution of sex-roles in the pheasant coucal Centropus phasianinus. Australian National University, Canberra

    Google Scholar 

  41. Maurer G (2007b) Love is in the air: arboreal copulations in the pheasant coucal Centropus phasianinus. North Territory Nat 19:48–50

    Google Scholar 

  42. Maurer G (2008) Who cares? Males provide most parental care in a monogamous nesting cuckoo. Ethology 114:540–547

    Article  Google Scholar 

  43. Maurer G, Hale ML, Verduijn MH, Wolff K (2005) Polymorphic microsatellite loci in pheasant coucal (Centropus phasianinus). Mol Ecol Notes 5:337–339

    Article  CAS  Google Scholar 

  44. Maurer G, Smith C, Süsser M, Magrath RD (2008) Solo and duet calling in the pheasant coucal: sex and individual call differences in a nesting cuckoo with reversed sexual size dimorphism. Aust J Zool 56:143–149

    Article  Google Scholar 

  45. Maurer G, Beck N, Double MC (2009) A ‘feather-trap’ for collecting DNA samples from birds. Mol Ecol Resour 10:129–134

    PubMed  Article  Google Scholar 

  46. Maynard Smith J (1977) Parental investment: a prospective analysis. Anim Behav 25:1–9

    Article  Google Scholar 

  47. Maynard Smith J (1978) The evolution of sex. Cambridge University Press, Cambridge

    Google Scholar 

  48. Michalek KG, Winkler H (2001) Parental care and parentage in monogamous great spotted woodpeckers (Picoides major) and middle spotted woodpeckers (Picoides medius). Behaviour 138:1259–1285

    Article  Google Scholar 

  49. Muck C, Kempenaers B, Kuhn S, Valcu M, Goymann W (2009) Paternity in the classical polyandrous black coucal (Centropus grillii)—a cuckoo accepting cuckoldry? Behav Ecol 20:1185–1193

    Article  Google Scholar 

  50. Nicholls JA, Double MC, Rowell DM, Magrath RD (2000) The evolution of cooperative and pair breeding in thornbills Acanthiza (Pardalotidae). J Avian Biol 31:165–176

    Article  Google Scholar 

  51. Nisbet ICT (1973) Courtship-feeding, egg-size and breeding success in common terns. Nature 241:141

    Article  Google Scholar 

  52. Oring LW, Lank DB (1986) Polyandry in spotted sandpipers: the impact of environment and experience. In: Rubenstein DR, Wrangham RW (eds) Ecological aspects of social evolution. Princeton University Press, Princeton, pp 21–42

    Google Scholar 

  53. Oring LW, Fleischer RC, Reed JM, Marsden KE (1992) Cuckoldry through stored sperm in the sequentially polyandrous spotted sandpiper. Nature 359:631–633

    Article  Google Scholar 

  54. Owens IPF (2002) Male-only care and classical polyandry in birds: phylogeny, ecology and sex differences in remating opportunities. Philos Trans R Soc Lond B 357:283–293

    Article  Google Scholar 

  55. Payne RB (2005) Bird families of the world: the Cuckoos. Oxford University Press, Oxford

    Google Scholar 

  56. Petrie M, Kempenaers B (1998) Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol Evol 13:52–58

    PubMed  Article  CAS  Google Scholar 

  57. Pierce EP, Lifjeld JT (1998) High paternity without paternity assurance behaviour in the purple sandpiper, a species with high paternal investment. Auk 115:602–612

    Google Scholar 

  58. Rahn H, Paganelli CV, Ar A (1975) Relation of avian egg weight to body weight. Auk 92:750–765

    Google Scholar 

  59. Ralph CP (1975) Life style of Coccyzus pumilus, a tropical cuckoo. Condor 77:60–72

    Article  Google Scholar 

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

    Article  Google Scholar 

  61. Slotow R (1996) Black coucal, Centropus grillii, egg volume predicts their polyandrous mating system. J Avian Biol 27:171–173

    Article  Google Scholar 

  62. Staicer CA, Spector DA, Horn AG (1996) The dawn chorus and other diel patterns in acoustic signalling. In: Kroodsma DE, Miller EH (eds) Ecology and evolution of acoustic comminucation in birds. Cornell University Press, Ithaca

    Google Scholar 

  63. Szekely T, Reynolds JD, Figuerola J (2000) Sexual size dimorphism in shorebirds, gulls, and alcids: the influence of sexual and natural selection. Evolution 54:1404–1413

    PubMed  CAS  Google Scholar 

  64. Taplin A, Beurteaux Y (1992) Aspects of the breeding biology of the pheasant coucal, Centropus phasianinus. Emu 92:141–146

    Article  Google Scholar 

  65. Trivers RL (1972) Parental investment and sexual selection. In: Cambell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179

    Google Scholar 

  66. Vernon CJ (1971) Notes on the biology of the black coucal. Ostrich 42:242–258

    Article  Google Scholar 

  67. Vincent A, Ahnesjo I, Berglund A, Rosenqvist G (1992) Pipefishes and seahorses: are they all sex role reversed? Trends Ecol Evol 7:237–241

    PubMed  Article  CAS  Google Scholar 

  68. Voigt C, Goymann W (2007) Sex-role reversal is reflected in the brain of African black coucals (Centropus grillii). Dev Neurobiol 67:1560–1573

    PubMed  Article  Google Scholar 

  69. Weising K, Wolff K, Nybom H, Meyer W (1995) DNA fingerprinting in plants and fungi. CRC, Boca Raton

    Google Scholar 

  70. Westneat DF, Sherman PW (1993) Parentage and the evolution of parental behavior. Behav Ecol 4:66–77

    Article  Google Scholar 

  71. Whitfield DP (1995) Behaviour and ecology of a polyandrous population of grey phalaropes Phalaropus fulicarius in Iceland. J Avian Biol 26:349–352

    Article  Google Scholar 

  72. Wright J (1998) Paternity and paternal care. In: Møller AP, Birkhead TR (eds) Sperm competition and sexual selection. Academic, San Diego, pp 117–145

    Google Scholar 

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Acknowledgments

We thank S. Musgrave, A. Quellmalz, S. Quinlan, C. Smith, M. Starling, R. Noske and W. Goymann with planning and conducting the fieldwork, and N. Beck, S. Cooney, N. Langmore and two anonymous reviewers for comments on earlier drafts. The study received support from the Stuart Leslie Bird Research Award, the Cayley Memorial Scholarship, the Ingram trust, and The North Australia Research Unit. The work was conducted under permits from Parks Northern Territory (16973) and the Ethics Committee of the Australian National University (F.BTZ.56.03) and complies with the laws and regulations of the Commonwealth of Australia.

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Correspondence to G. Maurer.

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Communicated by Douglas Robinson.

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Maurer, G., Double, M.C., Milenkaya, O. et al. Breaking the rules: sex roles and genetic mating system of the pheasant coucal. Oecologia 167, 413 (2011). https://doi.org/10.1007/s00442-011-2002-4

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Keywords

  • Extra-pair paternity
  • Parental care
  • Polyandry
  • Sex-role reversal
  • Sexual size dimorphism