Paternity in the classical polyandrous black coucal (Centropus grillii)-a cuckoo accepting cuckoldry?

Behavioral Ecology

Volumn 20, Issue 6, 2009, Pages 1185-1193

  Muck, Christina ^a   Kempenaers, Bart ^a   Kuhn, Sylvia ^a   Valcu, Mihai ^a   Goymann, Wolfgang ^a  

^a MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

Author keywords

African black coucal; Home range; Paternal care; Paternity; Polyandry; Sex role reversal

Indexed keywords

BIRD; CLUTCH SIZE; COPULATION; GENETIC MARKER; HOME RANGE; PATERNAL CARE; PATERNITY; POLYANDRY; SEX ROLE;

AVES; CENTROPUS GRILLII;

EID: 70450285246     PISSN: 10452249     EISSN: 14657279     Source Type: Journal    
DOI: 10.1093/beheco/arp118     Document Type: Article

References (81)

1. 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.
2. Anderson M. 2005. Evolution of classical polyandry: three steps to female emancipation. Ethology. 111:1-23.
3. Armour JA, Neumann R, Gobert S, Jeffreys AJ. 1994. Isolation of human simple repeat loci by hybridization selection. Hum Mol Genet. 3:599-605.
4. Arnqvist G, Kirkpatrick M. 2005. The evolution of infidelity in socially monogamous passerines: the strength of direct and indirect selection on extrapair copulation behaviour in females. Am Nat. 165: 26-37.
5. Birkhead TR. 1998. Sperm competition in birds. Rev Reprod. 3: 123-129.
6. Birkhead TR, Møller AP. 1992. Numbers and size of sperm storage tubules and the duration of sperm storage in birds: a comparative study. Biol J Linn Soc. 45:363-372.
7. Blumstein DT. 2000. The evolution of infanticide in rodents: a comparative analysis. In: Van Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge: Cambridge University Press. p. 178-197.
8. Boncoraglio G, Saino N. 2008. Barn swallow chicks beg more loudly when broodmates are unrelated. J Evol Biol. 21:256-262.
9. Börger L, Franconi N, De Michele G, Gantz A, Meschi F, Manica A, Lovari S, Coulson TIM. 2006. Effects of sampling regime on the mean and variance of home range size estimates. J Anim Ecol. 75:1393-1405.
10. Brooker MG, Rowley I, Adams M, Raverstock PR. 1990. Promiscuity: an inbreeding avoidance mechanism in a socially monogamous species? Behav Ecol Sociobiol. 26:191-199.
11. Calenge C. 2006. The package adehabitat for the R software: a tool for the analysis of space and habitat use by animals. Ecol Model. 197:516-519.
12. Clutton-Brock TH. 1991. The evolution of parental care. Princeton (NJ): Princeton University Press.
13. Chiver I, Stutchbury BJM, Morton ES. 2008. Do male plumage and song characteristics influence female off-territory forays and paternity in the hooded warbler? Behav Ecol Sociobiol. 62: 1981-1990.
14. Dale J, Montgomerie R, Michaud D, Boag P. 1999. Frequency and timing of extrapair fertilization in the polyandrous red phalarope (Phalaropus fulicarius). Behav Ecol Sociobiol. 46:50-56.
15. Davies NB. 1992. Dunnock behaviour and social evolution. Oxford: Oxford University Press.
16. 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.
17. Digby L. 2000. Infanticide by female mammals: implications for the evolution of social systems. In: Van Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge: Cambridge University Press. p. 423-446.
18. Double M, Cockburn A. 2000. Pre-dawn infidelity: females control extra-pair mating in superb fairy-wrens. Proc R Soc Lond B Biol Sci. 267:465-470.
19. Emlen ST, Oring LW. 1977. Ecology, sexual selection, and the evolution of mating systems. Science. 197:215-223.
20. Emlen ST, Wrege PH, Webster MS. 1998. Cuckoldry as a cost of polyandry in the sex-role-reversed wattled jacana, Jacana jacana. Proc R Soc Lond B Biol Sci. 265:2359-2364.
21. Ewen JG, Armstrong DP. 2000. Male provisioning is negatively correlated with attempted extrapair copulation frequency in the stitchbird (or hihi). Anim Behav. 60:429-433.
22. Freeman-Gallant CR. 1996. DNA fingerprinting reveals female preference for male parental care in Savannah sparrows. Proc R Soc Lond B Biol Sci. 263:157-160.
23. Frey R, Goymann W. Forthcoming. 2009. A single functional testis and long deferent duct papillae-the peculiar male reproductive tract of the classically polyandrous, sex-role reversed black coucal (Centropus grillii). J Ornithol. 10.1007/s10336-009-0403-405
24. Fridolfsson AK, Gyllenstein UB, Jakobsson S. 1997. Microsatellite markers for paternity testing in the Willow warbler Phylloscopus trochilus: high frequency of extra-pair young in an island population. Heredity. 126:127-132.
25. Gautschi B, Tenzer I, Müller JP, Schmid B. 2000. Isolation and characterization of microsatellite loci in the bearded vulture (Gypaetus barbatus) and crossamplifi cation in three Old World vulture species. Mol Ecol. 9:2193-2195.
26. Gautschi B, Widmer A, Koella J. 2000. Isolation and characterization of microsatellite loci in the dice snake (Natrix tessellata). Mol Ecol. 9:2191-2193.
27. Gowaty PA, Bridges WC. 1991. Behavioural, demographic, and environmental correlates of extra-pair fertilizations in eastern bluebirds, Sialia sialis. Behav Ecol. 2:339-350.
28. Goymann W. 2004. Wetteifernde Weibchen und fürsorgliche Männchen-Geschlechter-rollentausch beim Afrikanischen Grillkuckuck. Jahrb Max-Planck-Ges. 2004:513-518.
29. 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.
30. Goymann W, Wingfield JC. 2004. Competing females and caring males. II. Sex steroids in African black coucals, Centropus grilli. Anim Behav. 68:733-740. (Pubitemid 39348053)
31. Goymann W, Wittenzellner A, Schwabl I, Makomba M. 2008. Progesterone modulates aggression in sex-role reversed African black coucals. Proc R Soc Lond B Biol Sci. 275:1053-1060.
32. Goymann W, Wittenzellner A, Wingfield JC. 2004. Competing females and caring males. I. Polyandry and sex-role reversal in African black coucals, Centropus grillii. Ethology. 110:807-823. (Pubitemid 39428865)
33. Griffith SC. 2007. The evolution of infidelity in socially monogamous passerines: neglected components of direct and indirect selection. Am Nat. 169:274-280.
34. Griffith SC, Lyon BE, Montgomerie R. 2004. Quasi-parasitism in birds. Behav Ecol Sociobiol. 56:191-200.
35. 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.
36. Griffiths R, Double MC, Orr K, Dawson RJG. 1998. A DNA test to sex most birds. Mol Ecol. 7:1071-1075.
37. Gyllensten UB, Jakobsson S, Temrin H. 1990. No evidence for illegitimate young in monogamous and polygynous warblers. Nature. 343:168-170.
38. Haig SM, Mace TR, Mullins TD. 2003. Parentage and relatedness in polyandrous comb-crested jacanas using ISSRs. J Hered. 94:302-309.
39. Hoi-Leitner M, Hoi H, Romero-Pujante M, Valera F. 1999. Female extra-pair behaviour and environmental quality in the serin (Serinus serinus): a test of the 'constraint female hypothesis'. Proc R Soc Lond B Biol Sci. 266:1021-1026.
40. Houston AI. 1995. Parental effort and paternity. Anim Behav. 50: 1635-1644.
41. Houston AI, McNamara JM. 2002. A self-consistent approach to paternity and parental effort. Philos Trans R Soc Lond B Biol Sci. 357: 351-362.
42. Jennions MD, Petrie M. 2000. Why do females mate multiply? A review of the genetic benefits. Biol Rev. 75:21-64.
43. Kalinowski ST, Taper ML, Marshall TC. 2007. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol. 16:1099-1106.
44. Kempenaers B, Sheldon BC. 1997. Studying paternity and paternal care: pitfalls and problems. Anim Behav. 53:423-427.
45. Ketterson ED, Nolan V. 1994. Male parental behavior in birds. Annu Rev Ecol Syst. 25:601-628.
46. Johnstone RA, Hinde CA. 2006. Negotiation over offspring care-how should parents respond to each other's efforts? Behav Ecol. 17: 818-827.
47. Lifjeld JT, Slagsvold T, Ellegren H. 1998. Experimentally reduced paternity affects paternal effort and reproductive success in pied flycatchers. Anim Behav. 55:319-329.
48. Ligon JD. 1999. The evolution of avian breeding systems. Oxford: Oxford University Press.
49. Mauck RA, Marshall EA, Parker PG. 1999. Adult survival and imperfect assessment of parentage: effects on male parenting decision. Am Nat. 154:99-109.
50. Maurer G. 2007. Ecology and evolution of sex-roles in the pheasant coucal Centropus phasianinus [PhD thesis]. Canberra (Australia): The Australian National University.
51. Mee A, Whitfield DP, Thompson DBA, Burke T. 2004. Extrapair paternity in the common sandpiper, Actitis hypoleucos, revealed by DNA fingerprinting. Anim Behav. 67:333-342.
52. Mills JA. 1994. Extra-pair copulations in the red-billed gull-females with high quality, attentive males resist. Behaviour. 128:41-64.
53. Møller AP, Cuervo JJ. 2000. The evolution of paternity and paternal care in birds. Behav Ecol. 11:472-485.
54. 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 Biol Sci. 255:223-229.
55. Neff BD. 2003. Decisions about parental care in response to perceived paternity. Nature. 422:716-719.
56. Neff BD, Sherman PW. 2002. Decision making and recognition mechanisms. Proc R Soc Lond B Biol Sci. 269:1435-1441.
57. Oring LW, Fleischer RC, Reed JM, Marsden KE. 1992. Cuckoldry through stored sperm in the sequentially polyandrous spotted sandpiper. Nature. 39:631-633.
58. Owens IPF, Dixon A, Burke T, Thompson DBA. 1995. Strategic paternity assurance in the sex-role reversed Eurasian dotterel (Charadrius morinellus): behavioral and genetic evidence. Behav Ecol. 6:14-21.
59. Pandolfi M, Dastore PRP. 1994. Analysis of food-pass behavior in Montagu harrier Circus pygargus during the breeding period. Ethol Ecol Evol. 6:285-292.
60. Petrie M, Kempenaers B. 1998. Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol Evol. 13:52-58.
61. Petrie M, Lipsitch M. 1994. Avian polygyny is most likely in populations with high variability in heritable male fitness. Proc R Soc Lond B Biol Sci. 256:275-280.
62. Pierce EP, Lifjeld JT. 1998. High paternity without paternity-assurance behavior in the purple sandpiper, a species with high paternal investment. Auk. 115:602-612.
63. R Development Core Team. 2007. R: a language and environment for statistical computing [Internet]. Vienna (Austria): R Foundation for Statistical Computing. [cited 2009 June 25]. Available from: http://www.R-project.org.
64. Schamel D, Tracy DM, Lank DB, Westneat DF. 2004. Mate guarding, copulation strategies and paternity in the sex-role reversed, socially polyandrous red-necked phalarope Phalaropus lobatus. Behav Ecol Sociobiol. 57:110-118.
65. Schmoll T, Schurr FM, Winkel W, Epplen JT, Lubjuhn T. 2009. Lifespan, lifetime reproductive performance and paternity loss of within-pair and extra-pair offspring in the coal tit Periparus ater. Philos Trans R Soc Lond B Biol Sci. 276:337-345.
66. Schwagmeyer PL, Clair RCSt, Moodie JD, Lamey TC, Schnell GD, Moodie MN. 1999. Species differences in male parental care in birds: a reexamination of correlates with paternity. Auk. 116: 487-503.
67. Seutin G, White BN, Boag PT. 1991. Preservation of avian blood and tissue samples for DNA analysis. Can J Zool. 69:82-90.
68. Sheldon BC. 2002. Relating paternity to paternal care. Philos Trans R Soc B Biol Sci. 357:341-350.
69. Sheldon BC, Rasanen K, Dias PC. 1997. Certainty of paternity and paternal effort in the collard flycatcher. Behav Ecol. 8:421-428.
70. Trivers RL. 1972. Parental investment and sexual selection. In: Campbell B, editor. Sexual selection and the descent of man 1871-1971. Chicago (IL): Aldine. p. 136-179.
71. Veiga JP. 2004. Replacement female house sparrows regularly commit infanticide: gaining time or signaling status? Behav Ecol. 15: 219-222.
72. Vernon CJ. 1971. Notes on the biology of the black coucal. Ostrich. 42:242-257.
73. Wagner RH, Schug MD, Morton ES. 1996. Condition-dependent control of paternity by female purple martins: implications for coloniality. Behav Ecol Sociobiol. 38:379-389.
74. Westneat DF, Sargent RC. 1996. Sex and parenting: the effects of sexual conflict and parentage on parental strategies. Trends Ecol Evol. 11:87-91.
75. Westneat DF, Sherman PW. 1993. Parentage and the evolution of parental behavior. Behav Ecol. 4:66-77.
76. Westneat DF, Stewart IRK. 2003. Extra-pair paternity in birds: causes, correlates, and conflict. Annu Rev Ecol Evol Syst. 34:365-396.
77. Whittingham LA, Dunn PO. 1998. Male parental effort and paternity in a variable mating system. Anim Behav. 55:629-640.
78. Whittingham LA, Dunn PO. 2001. Male parental care and paternity in birds. Curr Ornithol. 16:257-298.
79. Whittingham LA, Taylor PD, Robertson RJ. 1992. Confidence of paternity and male parental care. Am Nat. 139:1115-1125.
80. Worton BJ. 1989. Kernel methods for estimating the utilization distribution in home-range studies. Ecology. 70:164-168.
81. Zuk M. 2002. Sexual selections. What we can and what we can't learn about sex from animals. Berkley (CA): University of California Press.