Abstract
Seabirds are long-lived birds that exhibit very high levels of parental investment, and male parental care is indispensable. Seabirds have comparable breeding and life history parameters, being colonial, long-lived, and exhibiting little or no sex dimorphism. It is thought that these characteristics explain why seabirds exhibit a uniformly low level of extra-pair paternity. However, among the relatively few seabirds that have been studied to date, some regularly engage in extra-pair copulations, and the reasons for such inter-specific variability remain unclear. We here analyse paternity in a small sub-Antarctic seabird, the Thin-billed Prions Pachyptila belcheri, using species-specific microsatellites as genetic markers. We found that 7 of 34 chicks (21%) were not fathered by the male pair partner. This value is among the highest recorded for seabirds, and it now needs to be established if these result from forced copulations as suggested for some albatross species, or female cuckoldry.
Zusammenfassung
Fremdvaterschaften bei Seevögeln: eine Übersicht und Fallstudie an Dünnschnabel-Walvögeln Pachyptila belcheri
Seevögel sind langlebig und zeigen ein hohes Maß an elterlichen Investitionen mit obligater Versorgung durch weibliche und mänchliche Elterntiere. Seevögel haben weiterhin vergleichbare Brut- und Life History-Parameter, so zum Beispiel Koloniebrüten, Langlebigkeit und schwachen oder keinen Geschlechtsdimorphismus. Man nimmt daher an, daß diese Charakteristika mit einem einheitlich niedrigen Maß an Fremdvaterschaften bei Seevögeln im Zusammenhamng stehen. Unter den relativ wenigen bisher untersuchten Seevögeln gibt es jedoch auch solche, bei denen regelmäßig Fremdvaterschaften beobachtet werden, und die Gründe für die zwischenartliche Variabilität sind bislang nicht geklärt. In der vorliegenden Arbeit untersuchen wir Vaterschaftsbeziehungen in einer kleinen subantarktischen Seevogelart, dem Dünnschnabel-Walvogel Pachyptila belcheri, mit Hilfe von artsprezifischen Mikrosatelliten als genetischen Markern. Wir fanden sieben Fremdvaterschften in 34 Küken bzw. Bruten (21%). Dieser Wert gehört zu den höchsten, die bei Seevögeln festgestellt wurden. In Folgeuntersuchungen sollte nun ermittelt werden, ob die Fremdvaterschaften das Ergebnis erzwungener Kopulationen sind, wie es für einige Albatrossarten vorgeschlagen wurde, oder ob Weibchen aktiv fremdgehen.
Similar content being viewed by others
References
Abbott CL, Double MC, Gales R, Cockburn A (2006) Copulation behaviour and paternity in shy albatrosses (Thalassarche cauta). J Zool 270:628–635
Anderson DJ, Boag PT (2006) No extra-pair fertilization observed in Nazca booby (Sula granti) broods. Wilson J Ornithol 118:244–247
Anker-Nilssen T, Kleven O, Aarvak T, Lifjeld JT (2008) No evidence of extra-pair paternity in the Atlantic puffin Fratercula arctica. Ibis 150:619–622
Anker-Nilssen T, Kleven O, Aarvak T, Lifjeld JT (2010) Low or no occurrence of extra-pair paternity in the black guillemot Cepphus grylle. J Ornithol 151:247–250
Austin JJ, Parkin DT (1995) Female-specific restriction fragments revealed by DNA fingerprinting and implications for extra-pair fertilizations in the short-tailed shearwater (Puffinus tenuirstris: Procellariiformes: Procellariidae). Aust J Zool 43:443–447
Baumgarten MM, Kohlrausch AB, Miyaki CY, de Freitas TRO, de Araujo AM (2001) DNA fingerprinting and parentage in masked (Sula dactylatra) and brown (S. leucogaster) boobies. Ornithol Neotrop 12:319–326
Birkhead TR, Hatchwell BJ, Lindner R, Blomqvist D, Pellatt EJ, Griffiths R, Lifjeld JT (2001) Extra-pair paternity in the common murre. Condor 103:158–162
Bukacińska M, Bukaciński D, Epplen JT, Sauer KP, Lubjuhn T (1998) Low frequency of extra-pair paternity in common gulls (Larus canus) as revealed by DNA fingerprinting. J Ornithol 139:413–420
Burg TM, Croxall JP (2006) Extrapair paternities in black-browed Thalassarche melanophris, grey-headed T. chrysostoma and wandering albatrosses Diomedea exulans at South Georgia. J Avian Biol 37:331–338
Cornwallis CK, West SA, Davis KE, Griffin AS (2010) Promiscuity and the evolutionary transition to complex societies. Nature 466:969–972
Dearborn DC, Anders AD, Parker PG (2001) Sexual dimorphism, extrapair fertilizations, and operational sex ratio in great frigatebirds (Fregata minor). Behav Ecol 12:746–752
Gilbert L, Burke T, Krupa A (1998) No evidence for extra-pair paternity in the western gull. Mol Ecol 7:1549–1552
Gonzáles-Solís J, Sokolov E, Becker PH (2001) Courtship feedings, copulations and paternity in common terns, Sterna hirundo. Anim Behav 61:1125–1132
Graves J, Hay RT, Scallan M, Rowe S (1992) Extra-pair paternity in the shag, Phalacrocorax aristotelis as determined by DNA fingerprinting. J Zool 226:399–408
Graves J, Ortega-Ruano J, Slater PJB (1993) Extra-pair copulations and paternity in shags: do females choose better males? Proc R Soc Lond B 253:3–7
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 71:219–222
Helfenstein F, Tirard C, Danchin E, Wagner RH (2004) Low frequency of extra-pair paternity and high frequency of adoption in black-legged kittiwakes. Condor 106:149–155
Hunter FM, Burke T, Watts SE (1992) Frequent copulation as a method of paternity assurance in the northern fulmar. Anim Behav 44:149–156
Huyvaert KP, Anderson DJ, Jones TC, Duan W, Parker PG (2000) Extra-pair paternity in waved albatrosses. Mol Ecol 9:1415–1419
Huyvaert KP, Anderson DJ, Parker PG (2006) The mate opportunity hypothesis and extra-pair paternity in waved albatrosses (Phoebastria irrorata). Auk 123:524–533
Ibarguchi G, Gissing GJ, Gaston AJ, Boag PT, Friesen VL (2004) Male-biased mutation rates and the overestimation of extrapair paternity: problem, solution, and illustration using thick-billed murres (Uria lomvia, Alcidae). J Hered 95:209–216
Jouventin P, Charmantier A, Dubois MP, Jarne P, Bried J (2007) Extra-pair paternity in the strongly monogamous wandering albatross Diomedea exulans has no apparent benefits for females. Ibis 149:67–78
Kempenaers B, Congdon B, Boag P, Robertson RJ, Boag PT (1999) Extrapair paternity and egg hatchability in tree swallows: evidence for the genetic compatibility hypothesis? Behav Ecol 10:304–311
Kingma SA, Hall ML, Segelbacher G, Peters A (2009) Radical loss of an extreme extra-pair mating system. BMC Ecol 9:15
Klauke N, Masello JF, Quillfeldt P, Segelbacher G (2009) Isolation of tetranucleotide microsatellite loci in the burrowing parrot (Cyanoliseus patagonus). J Ornithol 150:921–924
Lessios HA (1992) Testing electrophoretic data for agreement with Hardy-Weinberg expectations. Mar Biol 112:517–523
Ležalová-Piálková R (2011) Molecular evidence for extra-pair paternity and intraspecific brood parasitism in the black-headed gull. J Ornithol 152:291–295
Lifjeld JT, Harding AMA, Mehlum F, Oigarden T (2005) No evidence of extra-pair paternity in the little auk Alle alle. J Avian Biol 36:484–487
Lorentsen S, Amundsen T, Anthonisen K, Lifjeld J (2000) Molecular evidence for extrapair paternity and female-female pairs in a socially monogamous colonial seabird, the Antarctic petrel. Auk 117:1042–1047
Marshall TC, Slate J, Kruuk L, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655
Masello JF, Sramkova A, Quillfeldt P, Epplen JT, Lubjuhn T (2002) Genetic monogamy in burrowing parrots Cyanoliseus patagonus? J Avian Biol 33:99–103
Mauck RA, Waite TA, Parker PG (1995) Monogamy in Leach’s storm-petrel: DNA-fingerprinting evidence. Auk 112:473–482
Mauck RA, Marshall EA, Parker PG (1999) Adult survival and imperfect assessment of parentage: effects on male parenting decisions. Am Nat 154:99–109
McLean I, Kayes S, Murie J, Davis L, Lambert D (2000) Genetic monogamy mirrors social monogamy in the Fjordland crested penguin. NZ J Zool 27:311–316
Millar CD, Anthony I, Lambert DM, Stapleton PM, Bergmann CC, Bellamy AR, Young EC (1994) Patterns of reproductive success determined by DNA fingerprinting in a communally breeding oceanic bird. Biol J Linn Soc 52:31–48
Millar CD, Lambert DM, Young EC (1997) Minisatellite DNA detects sex, parentage, and adoption in the south polar skua. J Hered 88:235–238
Moreno J, Boto L, Fargallo J, de Leon A, Potti J (2000) Absence of extra-pair fertilisations in the chinstrap penguin Pygoscelis antartica. J Avian Biol 31:580–583
Pemberton JM, Slate J, Bancroft DR, Barrett JA (1995) Nonamplifying alleles at microsatellite loci: a caution for parentage and population studies. Mol Ecol 4:249–252
Petrie M, Kempenaers B (1998) Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol Evol 13:52–58
Piertney SB, Carss DN, Goostrey A (2003) Population variation in the frequency of extra-pair paternity in the great cormorant Phalacrocorax carbo. Vogelwelt 124(Suppl):149–155
Pilastro A, Pezzo F, Olmastroni S, Callegarin C, Corsolini S, Focardi S (2001) Extrapair paternity in the Adelie penguin Pygoscelis adeliae. Ibis 143:681–684
Quillfeldt P, Schmoll T, Peter H-U, Epplen JT, Lubjuhn T (2001) Genetic monogamy in Wilson’s storm-petrel. Auk 118:245–251
Quillfeldt P, Michalik A, Veit-Köhler G, Strange IJ, Masello JF (2010a) Inter-annual changes in diet and foraging trip lengths in a small pelagic seabird, the thin-billed prion Pachyptila belcheri. Mar Biol 157:2043–2050
Quillfeldt P, Voigt CC, Masello JF (2010b) Plasticity versus repeatability in seabird migratory behaviour. Behav Ecol Sociobiol 64:1157–1164
Quillfeldt P, Masello JF, McGill RAR, Adams M, Furness RW (2010c) Moving polewards in winter: a recent change in the migratory strategy of a pelagic seabird? Front Zool 7:15
Quillfeldt P, Masello JF, Poisbleau M, Chastel O, Schwabl I (2010d) Corticosterone at fledging depends on nestling condition, not on parental desertion. Open Access Anim Physiol 2:61–68
Rabouam C, Bretagnolle V, Bigot Y, Periquet G (2000) Genetic relationships of Cory’s shearwater: parentage, mating assortment, and geographic differentiation revealed by DNA fingerprinting. Auk 117:651–662
Schreiber EA, Burger J (eds) (2001) Biology of marine birds. CRC Press, Boca Raton
Schwartz MK, Boness DJ, Schaeff CM, Majluf P, Perry EA, Fleischer RC (1999) Female-solicited extrapair matings in Humboldt penguins fail to produce extrapair fertilizations. Behav Ecol 10:242–250
St Clair CC, Waas JR, St Clair RC, Boag PT (1995) Unfit mothers? Maternal infanticide in royal penguins. Anim Behav 50:1177–1185
Strange IJ (1980) The thin-billed prion, Pachyptila belcheri, at New Island, Falkland Islands. Gerfaut 70:411–445
Swatschek I, Ristow D, Wink M (1994) Mate fidelity and parentage in Cory’s shearwater Calonectris diomedea—field studies and DNA fingerprinting. Mol Ecol 3:259–262
Webster MS, Tarvin KA, Tuttle EM, Pruett-Jones S (2004) Reproductive promiscuity in the splendid fairy-wren: effects of group size and auxiliary reproduction. Behav Ecol 15:907–915
Wojczulanis-Jakubas K, Jakubas D, Oigarden T, Lifjeld JT (2009) Extrapair copulations are frequent but unsuccessful in a highly colonial seabird, the little auk, Alle alle. Anim Behav 77:433–438
Acknowledgments
The New Island Conservation Trust, Ian, Maria and Georgina Strange and Dan Birch facilitated fieldwork at New Island, which was approved and co-funded by the Falkland Islands Government (Environmental Planning Office). This study was funded by grants provided by the Deutsche Forschungsgemeinschaft DFG (Qu 148/1ff and SFB 454). We thank Katja Fleckenstein and Hendrika (Riek) van Noordwijk for technical assistance with genetic analyses and Sjouke Kingma for help with CERVUS paternity analyses. We are grateful to Jan T. Lifjeld and an anonymous referee for their helpful comments.
Conflict of interest
None.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by P. H. Becker.
Rights and permissions
About this article
Cite this article
Quillfeldt, P., Masello, J.F. & Segelbacher, G. Extra-pair paternity in seabirds: a review and case study of Thin-billed Prions Pachyptila belcheri . J Ornithol 153, 367–373 (2012). https://doi.org/10.1007/s10336-011-0751-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10336-011-0751-9