Behavioral Ecology and Sociobiology

, Volume 57, Issue 2, pp 110–118 | Cite as

Mate guarding, copulation strategies and paternity in the sex-role reversed, socially polyandrous red-necked phalarope Phalaropus lobatus

  • Douglas SchamelEmail author
  • Diane M. Tracy
  • David B. Lank
  • David F. Westneat
Original Article


In a recent review, Westneat and Stewart (2003) compiled evidence that extra-pair paternity results from a three-player interaction in which sexual conflict is a potent force. Sequentially polyandrous species of birds appear to fit this idea well. Earlier breeding males may attempt to use sperm storage by females to obtain paternity in their mate’s subsequent clutches. Later-breeding males may consequently attempt to avoid sperm competition by preferring to pair with previously unmated females. Females may bias events one way or the other. We examined the applicability of these hypotheses by studying mating behavior and paternity in red-necked phalaropes (Phalaropus lobatus), a sex-role reversed, socially polyandrous shorebird. Male red-necked phalaropes guarded mates more strongly than other shorebirds. Males increased within-pair copulation attempts during their mate’s fertile period, and maintained or further increased attempts towards the end of laying, suggesting an attempt to fertilize the female’s next clutch; these attempts were usually thwarted by the female. Paired males sought extra-pair copulations with females about to re-enter the breeding pool. Multilocus DNA fingerprinting showed that 6% of clutches (4/63) each contained one chick sired by a male other than the incubator, producing a population rate of these events of 1.7% (n=226 chicks). Male mates had full paternity in all first clutches (n=25) and 15 of 16 monogamous replacement clutches. In contrast, 3 of 6 clutches of second males contained extra-pair young likely fathered by the female’s previous mate. Previously mated female phalaropes may employ counter-strategies that prevent later mating males from discriminating against them. The stability of this polyandrous system, in which males provide all parental care, ultimately may depend on females providing males with eggs containing primarily genes of the incubating male, and not a previous mate.


DNA fingerprinting Paternity Phalaropus Polyandry Sex role reversal 



This manuscript has been improved by the useful comments of J. Dale, F. Cooke, L. Dill, R. Butler, J.D. Reynolds, W. Stein, P.D. O’Hara, and five anonymous reviewers. We thank D. Matkin, P. Klein, R. Gronquist, K. Oakley, L. Johnson, J. Cole, A. Swingley, C. Acevedo, Y. Zharikov, J. Schamel, and J.T. Schamel for field assistance. K. Wohl and B. Andres of US Fish and Wildlife Service, and D. Spirtes, R. Harris, L. Selig, and L. Dalle-Molle of Bering Land Bridge National Preserve provided logistical and financial support. We thank D. Blomqvist and co-workers for providing pre-publication paternity data on western sandpipers. Our paper is based upon work supported by the National Science Foundation, Office of Polar Programs, (grant OPP-9812841) through funding to process and analyze DNA samples; H. Mays, R. Hanschu, and T. Roush expedited that process. Additional funding came from Simon Fraser University, NOAA–OCSEAP, University of Alaska Natural Resources Fund, USGS–BRD, and the Frank M. Chapman Memorial Fund. This study was conducted under permits provided to D.S. and in accordance with the laws and ethical guidelines of the United States and Canada.


  1. Birkhead TR, Fletcher F (1995) Depletion determines sperm numbers in male zebra finches. Anim Behav 49:451–456CrossRefGoogle Scholar
  2. Birkhead TR, Møller AP (1992) Sperm competition in birds: evolutionary causes and consequences. Academic Press, LondonGoogle Scholar
  3. Birkhead TR, Møller AP (1996) Monogamy and sperm competition in birds. In: Black JM (ed) Partnerships in birds: the study of monogamy. Oxford University Press, Oxford, pp 323–343Google Scholar
  4. Birkhead TR, Veiga JP, Fletcher F (1993) Sperm competition and unhatched eggs in the house sparrow. J Avian Biol 26:343–345Google Scholar
  5. Birkhead TR, Martinez JG, Burke T, Froman DP (1999) Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc R Soc Lond B 266:1759–1764CrossRefPubMedGoogle Scholar
  6. Blomqvist D, Kempenaers B, Lanctot RB, Sandercock BK (2002) Genetic parentage and mate guarding in the arctic-breeding western sandpiper. Auk 119:228–233Google Scholar
  7. Briskie JV, Montgomerie R, Birkhead TR (1997) The evolution of sperm size in birds. Evolution 51:937–945Google Scholar
  8. Brown WD, Crespi, BJ, Choe JC (1997) Sexual conflict and the evolution of mating systems. In: Choe JC, Crespi BJ (eds) The evolution of mating systems in insects and arachnids. Cambridge University Press, Cambridge, pp 352–377Google Scholar
  9. Burke T, Davies NB, Bruford MW, Hatchwell BJ (1989) Parental care and mating behaviour of polyandrous dunnocks Prunella modularis related to paternity by DNA fingerprinting. Nature 338:249–251CrossRefGoogle Scholar
  10. Colegrave N, Birkhead TR, Lessells CM (1995) Sperm precedence in zebra finches does not require special mechanisms of sperm competition. Proc R Soc Lond B 259:223–228Google Scholar
  11. Colwell MA (1986) The first documented case of polyandry for Wilson’s phalarope (Phalaropus tricolor). Auk 103:611–612Google Scholar
  12. Colwell MA, Jehl JR Jr (1994) Wilson’s phalarope (Phalaropus tricolor). In: Poole A, Gill F (eds) The birds of North America, No 83. The Birds of North America, Philadelphia, Pa.Google Scholar
  13. Colwell MA, Oring LW (1989) Extra-pair mating in the spotted sandpiper: a female mate acquisition tactic. Anim Behav 38:675–684Google Scholar
  14. Dale J, Montgomerie R, Michaud D, Boag P (1999) Frequency and timing of extrapair fertilisation in the polyandrous red phalarope (Phalaropus fulicarius). Behav Ecol Sociobiol 46:50–56CrossRefGoogle Scholar
  15. Davies NB (1992) Dunnock behaviour and social evolution. Oxford University Press, OxfordGoogle Scholar
  16. Delehanty DJ, Fleischer RC, Colwell MA, Oring LW (1998) Sex-role reversal and the absence of extra-pair paternity in Wilson’s phalaropes. Anim Beh 55:995–1002CrossRefGoogle Scholar
  17. Dixon A, Ross D, O’Malley SLC, Burke T (1994) Paternal investment inversely related to degree of extra-pair paternity in the reed bunting. Nature 371:698–700CrossRefGoogle Scholar
  18. Dunn PO, Cockburn A (1996) Evolution of male parental care in a bird with almost complete cuckoldry. Evolution 50:2542–2548Google Scholar
  19. Dunn PO, Robertson RJ (1993). Extra-pair paternity in polygynous tree swallows. Anim Behav 45:231–239.CrossRefGoogle Scholar
  20. Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223PubMedGoogle Scholar
  21. Emlen ST, Wrege PH, Webster MS (1998) Cuckoldry as a cost of polyandry in the sex-role reversed wattled jacana. Proc R Soc Lond B 265:2359–2364CrossRefGoogle Scholar
  22. Fitch MA, Shugart GW (1984) Requirements for a mixed reproductive strategy in avian species. Am Nat 124:116–126CrossRefGoogle Scholar
  23. Gowaty PA (1996) Battles of the sexes and origins of monogamy. In: Black JM (ed) Partnerships in birds: the study of monogamy. Oxford University Press, Oxford, pp 11–19Google Scholar
  24. Griffith SC, Owens IPF, Thuman KA (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212CrossRefPubMedGoogle Scholar
  25. Hildén O, Vuolanto S (1972) Breeding biology of the Red-necked Phalarope Phalaropus lobatus in Finland. Ornis Fenn 49:57–85Google Scholar
  26. Johnsen A, Lifjeld JT, Rohde PA, Primmer CR, Ellegren H (1998) Sexual conflict over fertilizations: female bluethroats escape male paternity guards. Behav Ecol Sociobiol 43:401–408CrossRefGoogle Scholar
  27. Johnson DP, Briskie JV (1999) Sperm competition and sperm length in shorebirds. Condor 101:848–854Google Scholar
  28. Kålås JA, Byrkjadal I (1984) Breeding chronology and the mating system in the Eurasian dotterel (Charadrius morinellus). Auk 101:838–847Google Scholar
  29. Kempenaers B, Verheyen G, van den Broeck M, Burke T, van Broeckhoven C, Dhondt A (1992) Extra-pair paternity results from female preference for high-quality males in the blue tit. Nature 357:494–496CrossRefGoogle Scholar
  30. Ketterson ED, Nolan V Jr (1994) Male parental behavior in birds. Annu Rev Ecol Sys 25:601–628Google Scholar
  31. 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 266:2075–2081.CrossRefGoogle Scholar
  32. Lombardo MP (1998) On the evolution of sexually transmitted diseases in birds. J Avian Biol 29:314–321Google Scholar
  33. Mabee TJ, Estelle VB (2000) Assessing the effectiveness of predator exclosures for plovers. Wilson Bull 112:14–20Google Scholar
  34. Mays, HL (2001) Sexual conflict and constraints on female mating tactics in a monogamous passerine, the yellow-breasted chat. PhD thesis, University of Kentucky, LexingtonGoogle Scholar
  35. Mee, A, Whitfield DP, Thompson BA, Burke T (2004) Extra-pair paternity in the common sandpiper, Actitis hypoleucos, revealed by DNA fingerprinting. Anim Behav 67:333–342CrossRefGoogle Scholar
  36. Mehlum F (1991) The incubation behaviour of the grey phalarope Phalaropus fulicarius on Svalbard. Cinclus 14:33–37Google Scholar
  37. Michl G, Torok J, Griffith SC, Sheldon BC (2002) Experimental analysis of sperm competition mechanisms in a wild bird population. Proc Natl Acad Sci USA 99:5466–5470CrossRefPubMedGoogle Scholar
  38. Miller SA, Dykes DD, Polesky HF (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucl Acids Res 16:1215PubMedGoogle Scholar
  39. Møller AP (2000) Male parental care, female reproductive success, and extrapair paternity. Behav Ecol 11:161–168CrossRefGoogle Scholar
  40. Møller AP, Birkhead TR (1993) Certainty of paternity covaries with paternal care in birds. Behav Ecol Sociobiol 33:261–268Google Scholar
  41. Oring LW, Fleischer RC, Reed JM, Marsden KE (1992) Cuckoldry through stored sperm in the sequentially polyandrous spotted sandpiper. Nature 35:631–633CrossRefGoogle Scholar
  42. Oring LW, Reed JM, Maxson SJ (1994) Copulation patterns and mate guarding in the sex-role reversed, polyandrous spotted sandpiper. Anim Behav 47:1065–1072CrossRefGoogle Scholar
  43. 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 6:14–21Google Scholar
  44. Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567Google Scholar
  45. Pierce EP, Lifjeld JT (1998) High paternity without paternity-assurance behavior in the purple sandpiper, a species with high paternity investment. Auk 115:602–612Google Scholar
  46. Pizzari T, Cornwallis CK, Løvlie H, Jakobsson S, Birkhead TR (2003) Sophisticated sperm allocation in male fowl. Nature 426:70–74.CrossRefPubMedGoogle Scholar
  47. Reynolds JD (1987) Mating system and nesting biology of the red-necked phalarope Phalaropus lobatus: what constrains polyandry? Ibis 129:225–242Google Scholar
  48. Rubega MA, Schamel D, Tracy DM (2000) Red-necked phalarope (Phalaropus lobatus). In: Poole A, Gill F (eds) The birds of North America, No 538. The Birds of North America, Philadelphia, Pa.Google Scholar
  49. Sandercock BK (1998) Chronology of nesting events in western and semipalmated sandpipers near the Arctic Circle. J Field Ornithol 69:235–243Google Scholar
  50. SAS Institute (1999) SAS user’s guide: statistics, ver 8.00. SAS Institute, Cary, N.C.Google Scholar
  51. Schamel D (2000) Female and male reproductive strategies in the red-necked phalarope, a polyandrous shorebird. PhD thesis, Simon Fraser University, Burnaby, B.C.Google Scholar
  52. Schamel D, Tracy D (1977) Polyandry, replacement clutches, and site tenacity in the red phalarope (Phalaropus fulicarius) at Barrow, Alaska. Bird-Banding 48:314–324Google Scholar
  53. Schamel D, Tracy DM (1987) Latitudinal trends in breeding red phalaropes. J Field Ornithol 58:126–134Google Scholar
  54. Schamel D, Tracy DM, Lank DB (2004) Male mate choice, male availability, and egg production as limitations on polyandry in the red-necked phalarope. Anim Behav 67:847–853CrossRefGoogle Scholar
  55. Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90Google Scholar
  56. Smiseth PT, Amundsen T (1995) Female bluethroats (Luscinia s. svecica) regularly visit territories of extrapair males before egg laying. Auk 112:1049–1053Google Scholar
  57. Tracy DM, Schamel D, Dale J (2002) Red phalarope (Phalaropus fulicarius). In: Poole A, Gill F (eds) The birds of North America, No 698. The Birds of North America, Philadelphia, Pa.Google Scholar
  58. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179Google Scholar
  59. Westneat DF (1990) Genetic parentage in the indigo bunting: a study using DNA fingerprinting. Behav Ecol Sociobiol 27:67–76Google Scholar
  60. Westneat DF (1993) Polygyny and extrapair fertilizations in eastern red-winged blackbirds (Agelaius phoeniceus). Behav Ecol 4:49–60Google Scholar
  61. Westneat DF (1994) To guard mates or go forage: conflicting demands affect the paternity of male red-winged blackbirds. Am Nat 144:343–354CrossRefGoogle Scholar
  62. Westneat DF (2000) Toward a balanced view of the sexes: a retrospective and prospective view of genetics and mating patterns. In: Applolonio M, Festa-Bianchet M, Mainardi D (eds) Vertebrate mating systems. World Scientific, Singapore, pp 253–306Google Scholar
  63. Westneat DF, Rambo TB (2000) Copulation exposes female red-winged blackbirds to bacteria in male semen. J Avian Biol 31:1–7CrossRefGoogle Scholar
  64. Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: causes, correlates, and conflict. Annu Rev Ecol Evol Syst 34:365–396Google Scholar
  65. Wetton JH. Parkin DT (1991) An association between fertility and cuckoldry in the house sparrow, Passer domesticus. Proc R Soc Lond B 245:227–233Google Scholar
  66. Wetton JH, Carter RE, Parkin DT, Walters D (1987) Demographic study of a wild house sparrow population by DNA fingerprinting. Nature 327:147–149CrossRefPubMedGoogle Scholar
  67. Whitfield DP (1990) Male choice and sperm competition as constraints on polyandry in the red-necked phalarope Phalaropus lobatus. Behav Ecol Sociobiol 27:247–254Google Scholar
  68. Zharikov Y, Nol E (2000) Copulation behavior, mate guarding, and paternity in the semipalmated plover. Condor 102:231–235Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Douglas Schamel
    • 1
    Email author
  • Diane M. Tracy
    • 2
  • David B. Lank
    • 3
  • David F. Westneat
    • 4
  1. 1.Department of Biology and WildlifeUniversity of Alaska FairbanksFairbanksUSA
  2. 2.FairbanksUSA
  3. 3.Behavioral Ecology Research Group and Centre for Wildlife Ecology, Department of Biological SciencesSimon Fraser UniversityBurnabyCanada
  4. 4.Center for Ecology, Evolution, and Behavior, Department of BiologyUniversity of KentuckyLexingtonUSA

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