Abstract
It is still unclear why females in many bird species pursue extra-pair copulations. Current hypotheses focus mainly on indirect benefits such as obtaining particular “good genes” for their offspring or maximizing genetic compatibility between themselves and the father of their offspring. Supporting the latter, a recent study of shorebirds suggests that extra-pair matings may function to avoid the negative effects of genetic similarity between mates. Here, we further investigate genetic parentage in the Kentish plover, Charadrius alexandrinus, a shorebird with a highly variable social mating system. DNA fingerprinting revealed that most pairs were genetically monogamous: 7.9% of the broods (7/89) contained extra-pair young, comprising 3.9% of all chicks (9/229). These cases represented, however, three alternative reproductive behaviors: extra-pair paternity, quasi-parasitism (extra-pair maternity) and intraspecific brood parasitism. This is the first study showing the occurrence of all three behaviors in one shorebird species. We also found that extra-pair fertilizations (extra-pair paternity and quasi-parasitism) were more frequent later in the breeding season. There was no consistent relationship between genetic similarity of mates and laying date; the pattern, as well as the degree of genetic similarity, differed among breeding sites within the study population.
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References
Alves MAS, Bryant DM (1998) Brood parasitism in the sand martin, Riparia riparia: evidence for two parasitic strategies in a colonial passerine. Anim Behav 56:1323–1331
Amat JA, Fraga RM, Arroyo GM (1999) Brood desertion and polygamous breeding in the Kentish plover Charadrius alexandrinus. Ibis 141:596–607
Blomqvist D, Kempenaers B, Lanctot RB, Sandercock BK (2002a) Genetic parentage and mate guarding in the Arctic-breeding western sandpiper. Auk 119:228–233
Blomqvist D, Andersson M, Küpper C, Cuthill IC, Kis J, Lanctot RB, Sandercock BK, Székely T, Wallander J, Kempenaers B (2002b) Genetic similarity between mates and extra-pair parentage in three species of shorebirds. Nature 419:613–615
Blomqvist D, Andersson M, Küpper C, Cuthill IC, Kis J, Lanctot RB, Sandercock BK, Székely T, Wallander J, Kempenaers B (2003) Why do birds engage in extra-pair copulation? Reply. Nature 422:833–834
Brunton DH (1988) Sexual differences in reproductive effort: time-activity budgets of monogamous killdeer, Charadrius vociferus. Anim Behav 36:705–717
Cramp S, Simmons KEL (eds) (1983) The birds of the Western Palearctic, vol 3. Oxford University Press, Oxford
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 46:50–56
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
Ellegren H, Fridolfsson A-K (1997) Male-driven evolution of DNA sequences in birds. Nature Genet 17:182–184
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 265:2359–2364
Erckmann WJ (1983) The evolution of polyandry in shorebirds: an evaluation of hypotheses. In: Wasser SK (ed) Social behavior of female vertebrates. Academic Press, New York, pp 113–168
Foerster K, Delhey K, Johnsen A, Lifjeld JT, Kempenaers B (2003) Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:714–717
Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075
Griffith SC, Montgomerie R (2003) Why do birds engage in extra-pair copulation? Nature 422:833–834
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
Heg D, Ens BJ, Burke T, Jenkins L, Kruijt JP (1993) Why does the typically monogamous oystercatcher (Haematopus ostralegus) engage in extra-pair copulations? Behaviour 126:247–289
Hoi H, Hoi-Leitner M (1997) An alternative route to coloniality in the bearded tit: females pursue extra-pair fertilizations. Behav Ecol 8:113–119
Houston AI, McNamara JM (2002) A self-consistent approach to paternity and parental effort. Philos Trans R Soc Lond B 357:351–362
Johnson M, Beckmann JP, Oring LW (2002) Temperate breeding shorebirds copulate at night. Wader Study Group Bull 97:45–46
Krokene C, Anthonisen K, Lifjeld JT, Amundsen T (1996) Paternity and paternity assurance behaviour in the bluethroat, Luscinia s. svecica. Anim Behav 52:405–417
Kruuk LEB, Sheldon BC, Merilä J (2002) Severe inbreeding depression in collared flycatchers (Ficedula albicollis). Proc R Soc Lond B 269:1581–1589
Küpper C (2001) Frequency and timing of extra pair fertilizations in the polyandrous Kentish plover Charadrius alexandrinus. MSc Thesis, University of Vienna
Lanctot RB, Scribner KT, Kempenaers B, Weatherhead PJ (1997) Lekking without a paradox in the buff-breasted sandpiper. Am Nat 149:1051–1070
Lank DB, Smith CM, Hanotte O, Ohtonen A, Bailey S, Burke T (2002) High frequency of polyandry in a lek mating system. Behav Ecol 13:209–215
Lessells CM (1984) The mating system of Kentish plovers Charadrius alexandrinus. Ibis 126:474–483
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
Oring LW, Fleischer RC, Reed JM, Marsden KE (1992) Cuckoldry through stored sperm in the sequentially polyandrous spotted sandpiper. Nature 359:631–633
Oring LW, Reed JM, Maxson SJ (1994) Copulation patterns and mate guarding in the sex-role reversed, polyandrous spotted sandpiper, Actitis macularia. Anim Behav 47:1065–1072
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
Petrie M, Kempenaers B (1998) Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol Evol 13:52–58
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
Reeve HK, Westneat DF, Queller, DC (1992) Estimating average within-group relatedness from DNA fingerprints. Mol Ecol 1:223–232
Reyer HU, Bollmann K, Schläpfer AR, Schymainda A, Klecack G (1997) Ecological determinants of extrapair fertilizations and egg dumping in Alpine water pipits (Anthus spinoletta). Behav Ecol 8:534–543
Schleicher B, Hoi H, Valera F, Hoi-Leitner M (1997) The importance of different paternity guards in the polygynandrous penduline tit (Remiz pendulinus). Behaviour 134:941–959
Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90
Shin HS, Bargiello TA, Clark BT, Jackson FR, Young MW (1985) An unusual coding sequence from a Drosophila clock gene is conserved in vertebrates. Nature 317:445–448
Székely T, Cuthill IC (1999) Brood desertion in Kentish plover: the value of parental care. Behav Ecol 10:191–197
Székely T, Cuthill IC (2000) Trade-off between mating opportunities and parental care: brood desertion by female Kentish plovers. Proc R Soc Lond B 267:2087–2092
Székely T, Reynolds JD (1995) Evolutionary transitions in parental care in shorebirds. Proc R Soc Lond B 262:57–64
Székely T, Karsai I, Williams TD (1994) Determination of clutch-size in the Kentish plover Charadrius alexandrinus. Ibis 136:341–348
Székely T, Cuthill IC, Kis J (1999) Brood desertion in Kentish plover: sex differences in remating opportunities. Behav Ecol 10:185–190
Tregenza T, Wedell N (2002) Polyandrous females avoid costs of inbreeding. Nature 415:71–73
Václav R, Hoi H, Blomqvist D (2003) Food supplementation affects extrapair paternity in house sparrows (Passer domesticus). Behav Ecol 14:730–735
Wallander J, Blomqvist D, Lifjeld JT (2001) Genetic and social monogamy – does it occur without mate guarding in the ringed plover? Ethology 107:1–12
Westneat DF (1993) Polygyny and extrapair fertilizations in eastern red-winged blackbirds (Agelaius phoeniceus). Behav Ecol 4:49–60
Westneat DF, Sherman PW (1993) Parentage and the evolution of parental behavior. Behav Ecol 4:66–77
Westneat DF, Sherman PW (1997) Density and extra-pair fertilizations in birds: a comparative analysis. Behav Ecol Sociobiol 41:205–215
Wetton JH, Carter RE, Parkin DT (1987) Demographic study of a wild house sparrow population by DNA fingerprinting. Nature 327:147–149
Whittingham LA, Taylor PD, Robertson, RJ (1992) Confidence of paternity and male parental care. Am Nat 139:1115–1125
Yom-Tov Y (2001) An updated list and some comments on the occurrence of intraspecific nest parasitism in birds. Ibis 143:133–143.
Zharikov Y, Nol E (2000) Copulation behavior, mate guarding and paternity in the semipalmated plover. Condor 102:231–235
Acknowledgements
A. Johnsen, L. Oring, T. Pizzari, M. Webster and anonymous reviewers provided constructive comments on the manuscript. We also thank U. Bläsi and I. Moll (Vienna Biocenter) and K. Carter (Max Planck Research Centre for Ornithology, Seewiesen) for help with the laboratory work. The study was supported by the Konrad Lorenz Institute, Vienna, and by grants from NERC, UK (to I.C.C., A.I. Houston and J.M. McNamara, GR3/10957), the Hungarian Science Fund (to T.S., OTKA T031706), the Hungarian Ministry of Education (to T.S., FKFP-0470/2000) and the University of Veterinary Science, Budapest (to J.K., NKB-99-KUT-3-D/04). Rings were provided by the late Peter Evans (Durham University) and Radolfzell Vogelwarte, Germany. We are grateful to A. Lendvai, I. Szentirmai and Y. Demirhan for their assistance in the field. T. Yilmaz and S. Berberoglu (Çukurova University, Adana) and Ö. Karabaçak (National Park Authority, Adana) helped us with the logistics of the field work. Permissions for field work and blood sampling were provided by the Turkish Ministry for National Parks.
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Küpper, C., Kis, J., Kosztolányi, A. et al. Genetic mating system and timing of extra-pair fertilizations in the Kentish plover. Behav Ecol Sociobiol 57, 32–39 (2004). https://doi.org/10.1007/s00265-004-0832-3
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DOI: https://doi.org/10.1007/s00265-004-0832-3