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Extra-pair paternity in the black-headed gull: is it exceptional among colonial waterbirds?

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Although nesting at high densities promotes frequent interactions with individuals other than social mates, the rate of extra-pair paternity (EPP) in colonial waterbirds is generally low. So far, the highest EPP rate within this group has been reported in the black-headed gull Chroicocephalus ridibundus breeding in a colony in Czech Republic (33% broods with extra-pair offspring). In this study, we used a set of microsatellite loci to analyse parentage in 34 gull families (102 nestlings) from northern Poland. We recorded intra-specific brood parasitism in 10.8% of broods, but no evidence for EPP was found. The striking discrepancy between our results and previous estimates of EPP rate in the black-headed gull strongly indicate that promiscuity is a context-dependent strategy in this species and that its prevalence may greatly vary between populations. We recommend that a special care should be taken while using single-population data on EPP in the inter-specific comparative analyses.

Affiliations: 1: aDepartment of Biology and Animal Environment, Faculty of Animal Breeding and Biology, UTP University of Science and Technology, Mazowiecka 28, 85-084 Bydgoszcz, Poland ; 2: bDepartment of Biodiversity Studies and Bioeducation, Faculty of Biology and Environmental Protection, University of Łódź, Banacha 1/3, 90-237 Łódź, Poland

*Corresponding author’s e-mail address:

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1. Abbott C.L., Double M.C., Gales R., Cockburn A. (2006). "Copulation behaviour and paternity in shy albatrosses (Thalassarche cauta)". — J. Zool. Vol 270: 628-635. [Crossref]
2. Akçay E., Roughgarden J. (2007). "Extra-pair paternity in birds: review of the genetic benefits". — Evol. Ecol. Res. Vol 9: 855-868.
3. Anderson D.J., Boag P.T. (2006). "No extra-pair fertilization observed in Nazca booby (Sula granti) broods". — Wilson J. Ornithol. Vol 118: 244-247. [Crossref]
4. Anker-Nilssen T., Kleve O., Aarvak T., Lifjeld J.T. (2010). "Low or no occurrence of extra-pair paternity in the black guillemot Cepphus grylle". — J. Ornithol. Vol 151: 247-250. [Crossref]
5. Anker-Nilssen T., Kleven O., Aarvak T., Lifjeld J. (2008). "No evidence of extra-pair paternity in the Atlantic puffin Fratercula arctica". — Ibis Vol 150: 619-622. [Crossref]
6. Arct A., Drobniak S.M., Cichoń M. (2015). "Genetic similarity between mates predicts extrapair paternity — a meta-analysis of bird studies". — Behav. Ecol. Vol 26: 959-968. [Crossref]
7. Arnold K.E., Owens I.P.F. (2002). "Extra-pair paternity and egg dumping in birds: life history, parental care and the risk of retaliation". — Proc. Roy. Soc. Lond. B: Biol. Sci. Vol 269: 1263-1269. [Crossref]
8. Arnqvist G., Kirckpatrick M. (2005). "The evolution of infidelity in socially monogamous passerines: the strength of direct and indirect selection on extrapair copulation behaviuor in females". — Am. Nat. Vol 195(Suppl. 5): S26-S37. [Crossref]
9. Austin J.J., Parkin D.T. (1996). "Low frequency of extra-pair paternity in two colonies of the socially monogamous short-tailed shearwater Puffinus tenuirostris". — Mol. Ecol. Vol 5: 145-150. [Crossref]
10. Baião P.C., Parker P.G. (2009). "No evidence of extra-pair fertilization in red-footed boobies (Sula sula)". — Waterbirds Vol 32: 179-182. [Crossref]
11. Baumgarten M.M., Kohlrausch A.B., Miyaki C.Y., Ochotorena de Freitas T.R., Mellender de Araújo A. (2001). "DNA fingerprinting and parentage in masked (Sula dactylatra) and brown (S. leucogaster) boobies". — Ornitol. Neotrop. Vol 12: 319-326.
12. Birkhead T.R., Hunter F.M., Pellatt J.E. (1989). "Sperm competition in the zebra finch, Taeniopygia guttata". — Anim. Behav. Vol 38: 935-950. [Crossref]
13. Bouwman K.M., Komdeur J. (2006). "Weather conditions affect levels of extra-pair paternity in the reed bunting Emberiza schoeniclus". — J. Avian Biol. Vol 37: 238-244. [Crossref]
14. Bried J., Dubois M.P., Jarne P., Jouventin P., Santos R.S. (2010). "Does competition for nests affect genetic monogamy in Cory’s shearwater Calonectris diomedea?" — J. Avian. Biol. Vol 41: 407-418. [Crossref]
15. Bukacińska M., Bukaciński D., Epplen J.T., Sauer K.P., Lubjuhn T. (1998). "Low frequency of extra-pair paternity in common gulls (Larus canus) as revealed by DNA fingerprinting". — J. Ornithol. Vol 139: 413-420. [Crossref]
16. Burg M.T., Croxall P.J. (2006). "Extrapair paternities in black-browed Thalassarche melanophris, grey-headed T. chrysostoma and wandering albatrosses Diomedea exulans at south Georgia". — J. Avian Biol. Vol 37: 331-338. [Crossref]
17. Calderón L., Svagelj W.S., Quintana F., Lougheed S.C., Tubaro P.L. (2011). "No evidence of extra-pair paternity or intraspecific brood parasitism in the imperial shag Phalacrocorax atriceps". — J. Ornithol. Vol 153: 399-404. [Crossref]
18. Charmantier A., Blondel J. (2003). "A contrast in extra-pair paternity levels on mainland and island populations of Mediterranean blue tits". — Ethology Vol 109: 351-363. [Crossref]
19. Chuang-Dobbs H.C., Webster M.S., Holmes R.T. (2001). "The effectiveness of mate guarding by male black-throated blue warblers". — Behav. Ecol. Vol 12: 541-546. [Crossref]
20. Dearborn D.C., Anders A.D., Parker P.G. (2001). "Sexual dimorphism, extrapair fertilizations, and operational sex ratio in great frigatebirds (Fregata minor)". — Behav. Ecol. Vol 12: 746-752. [Crossref]
21. Dixon A., Ross D., O’Malley S.L.C., Burke T. (1994). "Paternal investment inversely related to degree of extra-pair paternity in the reed bunting". — Nature Vol 371: 698-700. [Crossref]
22. Dunn P.O., Afton A.D., Gloutney M.L., Alisauskas R.T. (1999). "Forced copulation results in few extrapair fertilizations in Ross’s and lesser snow geese". — Anim. Behav. Vol 57: 1071-1081. [Crossref]
23. Excoffier L., Lischer H.E.L. (2010). "Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows". — Mol. Ecol. Res. Vol 10: 564-567. [Crossref]
24. Forstmeier W., Nakagawa S., Griffith S.C., Kempenaers B. (2014). "Female extra-pair mating: adaptation of genetic constraint?" — Trends Ecol. Evol. Vol 29: 456-464. [Crossref]
25. Fridolfsson A.K., Ellegren H. (1999). "A simple and universal method for molecular sexing of nonratite birds". — J. Avian Biol. Vol 30: 116-121. [Crossref]
26. Gilbert L., Burke T., Krupa A. (1998). "No evidence for extra-pair paternity in the western gull". — Mol. Ecol. Vol 7: 1549-1552. [Crossref]
27. Given A.D., Mills J.A., Baker A.J. (2002). "Isolation of polymorphic microsatellite loci from the red-billed gull (Larus novaehollandiae scopulinus) and amplification in related species". — Mol. Ecol. Notes Vol 2: 416-418. [Crossref]
28. González-Solís J., Sokolov E., Becker P.H. (2001). "Courtship feedings, copulations and paternity in the common terns, Sterna hirundo". — Anim. Behav. Vol 61: 1125-1132. [Crossref]
29. Gowaty P. (1996). "Battles of the exes and origins of monogamy". — In: Partnerships in birds ( Black J.M., ed.). Oxford University Press, Oxford, p.  21-52.
30. Graves J., Ortega-Ruano J., Slater P.J.B. (1993). "Extra-pair copulations and paternity in shags: do females choose better males?" — Proc. Roy. Soc. Lond. B: Biol. Sci. Vol 253: 3-7. [Crossref]
31. Griffith S.C., Owens I.P.F., Thuman K.A. (2002). "Extra pair paternity in birds: a review of interspecific variation and adaptive function". — Mol. Ecol. Vol 11: 2195-2212. [Crossref]
32. Griffith S.C., Stewart I.R.K., Dawson D.A., Owens I.P.F., Burke T. (1999). "Contrasting levels of extra-pair paternity in mainland and island populations of the house sparrow (Passer domesticus): is there an ‘island effect’?" — Biol. J. Linn. Soc. Vol 68: 303-316.
33. Griffiths R., Double M.C., Orr K., Dawson R.J. (1998). "A DNA test to sex most birds". — Mol. Ecol. Vol 7: 1071-1075. [Crossref]
34. Griggio M., Matessi G., Marin G. (2004). "No evidence of extra-pair paternity in a colonial seabird, the common tern (Sterna hirundo)". — Ital. J. Zool. Vol 71: 219-222. [Crossref]
35. Guo S.W., Thompson E.A. (1992). "Performing the exact test of Hardy–Weinberg proportion for multiple alleles". — Biometrics Vol 48: 361-372. [Crossref]
36. Hammers M., von Engelhardt N., Langmore N.E., Komdeur J., Griffith S.C., Magrath M.J.L. (2009). "Mate-guarding intensity increases with breeding synchrony in the colonial fairy martin, Petrochelidon ariel". — Anim. Behav. Vol 78: 661-669. [Crossref]
37. Hasegwa M., Arai E., Kojima W., Kitamura W., Fujita G., Higuchi H., Watanabe M., Nakamura M. (2010). "Low level of extra-pair paternity in a population of the barn swallow Hirundo rustica gutturalis". — Ornithol. Sci. Vol 9: 161-164. [Crossref]
38. Helfenstein F., Tirard C., Danchin É., Wagner R.H. (2004). "Low frequency of extra-pair paternity and high frequency of adoption in black-legged kittiwakes". — Condor Vol 106: 149-155. [Crossref]
39. Hoi-Leitner M., Hoi H., Romero-Pujante M., Valera F. (1999). "Female extra-pair behavior and environmental quality in the serin (Serinus serinus): a test of the ‘constrained female hypothesis’". — Proc. Roy. Soc. Lond. B: Biol. Sci. Vol 266: 1021-1026. [Crossref]
40. Hsu Y.-H., Schroeder J., Winney I., Burke T., Nakagawa S. (2014). "Costly infidelity: low lifetime fitness of extra-pair offspring in a passerine bird". — Evolution Vol 68: 2873-2884. [Crossref]
41. Hunter F.M., Burke T., Watts S.E. (1992). "Frequent copulation as a method of paternity insurance in the northern fulmar". — Anim. Behav. Vol 44: 149-156. [Crossref]
42. Huyvaert K.P., Anderson D.J., Jones T.C., Duan W., Parker P.C. (2000). "Extra-pair paternity in waved albatrosses". — Mol. Ecol. Vol 9: 1415-1419. [Crossref]
43. Ibarguchi G., Gissing G.J., Gaston A.J., Boag P.T., Friesen V.L. (2004). "Male-biased mutation rates and the overestimation of extrapair paternity: problem, solution, and illustration using thick-billed murres (Uria lomvia, Alcidae)". — J. Hered. Vol 95: 209-216. [Crossref]
44. Jouventin P., Charmantier A., Dubois M.-P., Jarne P., Bried J. (2007). "Extra-pair paternity in the strongly monogamous wandering albatross Diomedea exulans has no apparent benefits for females". — Ibis Vol 149: 67-78. [Crossref]
45. Kalinowski S.T., Taper M.L., Marshall T.C. (2007). "Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment". — Mol. Ecol. Vol 16: 1099-1106. [Crossref]
46. Kalinowski S.T., Wagner A.P., Taper M.L. (2006). "ML-relate: a computer program for maximum likelihood estimation of relatedness and relationship". — Mol. Ecol. Notes Vol 6: 576-579. [Crossref]
47. Kempenaers B. (2007). "Mate choice and genetic quality: a review of the heterozygosity theory". — Adv. Study Behav. Vol 37: 189-278. [Crossref]
48. Ležalová-Piálková R. (2011). "Molecular evidence for extra-pair paternity and intra-specific brood parasitism in the black-headed gull". — J. Ornithol. Vol 152: 291-295. [Crossref]
49. Lifjeld J.T., Harding A.M.A., Mehlum F., Øigarden T. (2005). "No evidence of extra-pair paternity in the little auk Alle alle". — J. Avian Biol. Vol 36: 484-487. [Crossref]
50. Lopes I.F., Miño C.I., Rocha C.D., Oliveira D.M.M., De Lama S.N. (2013). "Inferred kinship patterns reveal low levels of extra-pair paternity in the endangered neotropical jabiru stork (Jabiru mycteria, Aves: Ciconiiformes)". — Genetica Vol 141: 195-203. [Crossref]
51. Lorentsen S.H., Amundsen T., Anthonisen K., Lifjeld J.T. (2000). "Molecular evidence for extra-pair paternity and female–female pairs in Antarctic petrels". — Auk Vol 117: 1042-1047. [Crossref]
52. Magrath M.J.L., Komdeur J. (2003). "Is male care compromised by additional mating opportunity." — Trends Ecol. Evol. Vol 18: 424-430. [Crossref]
53. Marthinsen G., Kleven O., Brenna E., Lifjeld J.T. (2005). "Part-time mate guarding affects paternity in male reed buntings (Emberiza schoeniclus)". — Ethology Vol 111: 397-409. [Crossref]
54. Mauck R.A., Marschall E.A., Parker P.G. (1999). "Adult survival and imperfect assessment of parentage: effects on male parenting decisions". — Am. Nat. Vol 154: 99-109. [Crossref]
55. Mauck R.A., Waite T.A., Parker P.G. (1995). "Monogamy in Leach’s storm-petrel: DNA fingerprinting evidence". — Auk Vol 112: 473-482. [Crossref]
56. McLean I., Kayes S., Murie J., Davis L., Lambert D. (2000). "Genetic monogamy mirrors social monogamy in the Fjordland crested penguin". — New Zeal. J. Zool. Vol 27: 311-316. [Crossref]
57. Meek S.B., Robertson R.J. (1994). "Interspecific competition for nestboxes affects mate guarding in eastern bluebirds, Sialia sialis". — Anim. Behav. Vol 47: 295-302. [Crossref]
58. Millar C.D., Anthony I., Lambert D., Stapleton P., Bergmann C., Bellamy A., Young E. (1994). "Patterns of reproductive success determined by DNA fingerprinting in a communally breeding oceanic bird". — Biol. J. Linn. Soc. Vol 52: 31-48. [Crossref]
59. Millar C.D., Lambert D.M., Young E.C. (1997). "Minisatellite DNA detects sex, parentage, and adoption in the south polar skua". — J. Hered. Vol 88: 235-238. [Crossref]
60. Minias P., Minias A., Dziadek J. (2014). "Occurrence of extra-pair paternity and intraspecific brood parasitism in the whiskered tern Chlidonias hybrida". — Bird Study Vol 61: 130-134. [Crossref]
61. Minias P., Wojczulanis-Jakubas K., Rutkowski R., Kaczmarek K., Janiszewski T. (2016). "Spatial patterns of extra-pair paternity in a waterbird colony: separating the effects of nesting density and nest site location". — Behav. Ecol. Sociobiol. Vol 70: 369-376. [Crossref]
62. Miño C.I., Russello M.A., Mussi Goncalves P.F., Del Lama S.N. (2011). "Reconstructing genetic mating systems in the absence of parental information in colonially breeding waterbirds". — BMC Evol. Biol. Vol 11: 196. [Crossref]
63. Møller A.P. (2000). "Male parental care, female reproductive success, and extrapair paternity". — Behv. Ecol. Vol 11: 161-168. [Crossref]
64. Møller A.P., Birkhead T.R. (1993). "Cuckoldry and sociality: a comparative study of birds". — Am. Nat. Vol 142: 118-140. [Crossref]
65. Møller A.P., Ninni P. (1998). "Sperm competition and sexual selection: a meta-analysis of paternity studies of birds". — Behav. Ecol. Sociobiol. Vol 43: 345-358. [Crossref]
66. Moreno J., Boto L., Fargallo J.A., de Léon A., Potti J. (2000). "Absence of extra-pair fertilisations in the chinstrap penguin Pygoscelis antarctica". — J. Avian Biol. Vol 31: 580-583. [Crossref]
67. Morton E.S., Forman L., Braun M. (1990). "Extrapair fertilizations and the evolution of colonial breeding in purple martins". — Auk Vol 107: 275-283. [Crossref]
68. Morton E.S., Stutchbury B.J.M., Howlett J.S., Piper W.H. (1998). "Genetic monogamy in blue-headed vireos and a comparison with a sympatric vireo with extra-pair paternity". — Behav. Ecol. Vol 9: 515-524. [Crossref]
69. Mougeot F. (2004). "Breeding density, cuckoldry risk and copulation behaviour during the fertile period in raptors: a comparative analysis". — Anim. Behav. Vol 67: 1067-1076. [Crossref]
70. Petrie M., Doums C., Møller A.P. (1998). "The degree of extra-pair paternity increases with genetic variability". — Proc. Natl Acad. Sci. USA Vol 95: 9390-9395. [Crossref]
71. Piertney S.B., Carss D.N., Goostrey A. (2003). "Population variation in the frequency of extra-pair paternity in the great cormorant". — Vogelwelt Vol 124(Suppl.): 149-155.
72. Pilastro A., Griggio M., Biddau L., Mingozzi T. (2002). "Extrapair paternity as a cost of polygyny in the rock sparrow: behavioural and genetic evidence of the ‘trade-off’ hypothesis". — Anim. Behav. Vol 63: 967-974. [Crossref]
73. Pilastro A., Pezzo F., Olmastroni S., Callegarin C., Corsolini S., Focardi S. (2001). "Extrapair paternity in the Adélie penguin Pygoscelis adeliae". — Ibis Vol 143: 681-684. [Crossref]
74. Puurtinen M., Ketola T., Kotiaho J.S. (2009). "The good-genes and compatible-genes benefits of mate choice". — Am. Nat. Vol 174: 741-752. [Crossref]
75. Quillfeldt P., Masello J.F., Segelbacher G. (2012). "Extra-pair paternity in seabirds: a review and case study of thin-billed prions Pachyptila belcheri". — J. Ornithol. Vol 153: 367-373. [Crossref]
76. Quillfeldt P., Schmoll T., Peter H.U., Eppeln J.T., Lubjuhn T. (2001). "Genetic monogamy in Wilson’s storm-petrel". — Auk Vol 118: 242-248. [Crossref]
77. Rabouam C., Bretagnolle V., Bigot Y., Périquet G. (2000). "Genetic relationships of Cory’s shearwater: parentage, mating assortment, and geographic differentiation revealed by DNA fingerprinting". — Auk Vol 117: 651-662. [Crossref]
78. Ramos A.G., Nunziata S.O., Lance S.L., Rodríguez C., Faircloth B.C., Gowaty P.A., Drummond H. (2014). "Habitat structure and colony structure constrain extrapair paternity in a colonial seabird". — Anim. Behav. Vol 95: 121-127. [Crossref]
79. Schwartz M.K., Boness D.J., Schaeff C.M., Majluf P., Perry E.A., Fleischer R.C. (1999). "Female-solicited extrapair matings in Humboldt penguins fail to produce extrapair fertilizations". — Behav. Ecol. Vol 10: 242-250. [Crossref]
80. Shealer D.A., Devbhandari S., Garcia-Mendoza M.G. (2014). "Evidence for genetic monogamy but low mate retention in the North American black tern (Chlidonias niger surinamensis)". — Waterbirds Vol 37: 129-135. [Crossref]
81. St Clair C.C., Waas J.R., St Clair R.C., Boag P.T. (1995). "Unfit mothers? Maternal infanticide in royal penguins". — Anim. Behav. Vol 50: 1177-1185. [Crossref]
82. Stewart S.L., Westneat D.F., Ritchison G. (2010). "Extra-pair paternity in eastern bluebirds: effects of manipulated density and natural patterns of breeding synchrony". — Behav. Ecol. Sociobiol. Vol 64: 463-473. [Crossref]
83. Stutchbury B.J.M., Morton E.S. (1995). "The effect of breeding synchrony on extra-pair mating systems in songbirds". — Behaviour Vol 132: 675-690. [Crossref]
84. Swatschek I., Ristow D., Wink M. (1994). "Mate fidelity and parentage in Cory’s shearwater Calonectris diomedea — field studies and DNA fingerprinting". — Mol. Ecol. Vol 3: 259-262. [Crossref]
85. Turjeman S.F., Centeno-Cuadros A., Eggers U., Rotics S., Blas J., Fiedler W., Kaatz M., Jeltsch F., Wikelski M., Nathan R. (2016). "Extra-pair paternity in the socially monogamous white stork (Ciconia ciconia) is fairly common and independent of local density". — Sci. Rep. Vol 6: 27976. [Crossref]
86. van Oosterhout C., Hutchinson W.F., Wills D.P., Shipley P. (2004). "Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data". — Mol. Ecol. Res. Vol 4: 535-538.
87. Westneat D.F., Sargent R.G. (1996). "Sex and parenting: the effects of sexual conflict and parentage on parental strategies". — Trends Ecol. Evol. Vol 11: 87-91. [Crossref]
88. Westneat D.F., Sherman P.W. (1997). "Density and extra-pair fertilizations in birds: a comparative analysis". — Behav. Ecol. Sociobiol. Vol 41: 205-215. [Crossref]
89. Westneat D.F., Sherman P.W., Morton M.L. (1990). "The ecology and evolution of extra-pair copulations in birds". — Curr. Ornithol. Vol 7: 331-369.
90. Westneat D.F., Stewart I.R.K. (2003). "Extra-pair paternity in birds: causes, correlates, and conflict". — Annu. Rev. Ecol. System. Vol 34: 365-396. [Crossref]
91. Wink M., Dyrcz A. (1999). "Mating systems in birds: a review of molecular studies". — Acta Ornithol. Vol 34: 91-109.
92. Wojczulanis-Jakubas K., Jakubas D., Øigarden T., Lifjeld J.T. (2009). "Extra-pair copulations are frequent but unsuccessful in a highly colonial seabird, the little auk Alle alle". — Anim. Behav. Vol 17: 433-438. [Crossref]
93. Yuta T., Koizumi I. (2016). "Does nest predation risk affect the frequency of extra-pair paternity in a socially monogamous passerine". — J. Avian Biol. Vol 47: 153-158. [Crossref]

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