Abstract
Genetic techniques have revealed surprisingly high rates of extra-pair paternity (EPP) in socially monogamous albatrosses. We sought to establish social and genetic influences on EPP in wandering albatrosses (Diomedea exulans) at Marion Island, where EPP rates were 14–24 % in three successive seasons. EPP probably resulted from both female solicited extra-pair behaviours and male forced copulations. EPP was not linked to breeding experience nor with poor reproductive performance, despite a tendency for pairs to consistently produce either EPP or within-pair paternity (WPP) chicks. Mate guarding may inhibit extra-pair behaviour; however, parental arrival date and presence in the colony prior to laying did not correlate with EPP. There was little support for genetic advantages to producing EPP chicks, but the population is characterised by low genetic variability, which may result in mate incompatibility. Mates of pairs that failed and pairs producing EPP young tended to be more similar genetically to their partners than mates producing WPP young, suggesting that EPP may counter mate incompatibility. EPP and WPP chicks grow equally well, so cuckolded males did not reduce investment in EPP chicks. The lack of discriminatory behaviour by cuckolded males together with low genetic diversity in the population may allow continued high levels of EPP. In albatrosses, pair bonds are typically long lasting and the costs of forming new pairings may discourage mate swapping. Females may undertake extra-pair copulations as an adaptive alternative to mate swapping because the costs of extra-pair behaviour are small.
This is a preview of subscription content, access via your institution.


References
Abbott CL, Double MC (2003) Genetic structure, conservation genetics and evidence of speciation by range expansion in shy and white-capped albatrosses. Mol Ecol 12:2953–2962
Abbott CL, Double MC, Cockburn A (2006) Copulation behaviour and paternity in shy albatrosses (Thalassarche cauta). J Zool 270:628–635
Amos W, Worthington Wilmer J, Fullard K, Burg TM, Croxall JP, Bloch D, Coulson T (2001) The influence of parental relatedness on reproductive success. Proc R Soc Lond B 268:2021–2027
Aparicio JM, Ortego J, Cordero PJ (2006) What should we weigh to estimate heterozygosity, alleles or loci? Mol Ecol 15:4659–4665
Birkhead TR, Møller AP (1992) Sperm competition in birds. Evolutionary causes and consequences. Academic, Cambridge
Blomqvist D, Andersson M, Küpper C, Cuthill IC, Kis J, Lanctot RB, Sandercock BK, Székely T, Wallander J, Kempenaers B (2002) Genetic similarity between mates and extra-pair parentage in three species of shorebirds. Nature 419:613–615
Bried J, Jouventin P (2002) Site and mate choice in seabirds: an evolutionary approach. In: Schreiber EA, Burger J (eds) Biology of marine birds. CRC, Boca Raton, pp 263–306
Bried J, Nicolaus M, Jarne P, Dubois M-P, Jouventin P (2007) Population biology of the wandering albatross (Diomedea exulans) in the Crozet and Kerguelen archipelagos, southern Indian Ocean, approached through genetic and demographic methods. J Zool 272:20–29
Brown JL (1997) A theory of mate choice based on heterozygosity. Behav Ecol 8:60–65
Brown CR, Adams NJ (1984) Female wandering albatross Diomedea exulans raising a chick on its own at Marion Island. Cormorant 12:103–104
Burg TM (1999) Primer Notes. Isolation and characterization of microsatellites in albatrosses. Mol Ecol 8:338
Burg TM, Croxall JP (2004) Global population structure and taxonomy of the wandering albatross species complex. Mol Ecol 13:2345–2355
Burg TM, Croxall JP (2006) Extrapair paternities in black-browed Thalassarche melanophris, grey-headed T. chrysostoma and wandering albatross Diomedea exulans at South Georgia. J Avian Biol 37:331–338
Chastel O, Weimerskirch H, Jouventin P (1995) Influence of body condition on reproductive decision and reproductive success in the blue petrel. Auk 112:964–972
Cohas A, Allainé D (2009) Social structure influences extra-pair paternity in socially monogamous mammals. Biol Lett 5:313–316
Crawley MJ (2008) The R book. Wiley, Chichester
R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. www.R-project.org
Dubois F, Wajnberg É, Cézilly F (2004) Optimal divorce and re-mating strategies for monogamous female birds: a simulation model. Behav Ecol Sociobiol 56:228–236
Dubois M-P, Jarne P, Jouventin P (2005) Ten polymorphic microsatellite markers in the wandering albatross Diomedea exulans. Mol Ecol Notes 14:905–907
Fietz J, Zischler H, Schwiegk C, Tomiuk J, Dausmann KH, Ganzhorn JU (2000) High rates of extra-pair young in the pair-living fat-tailed dwarf lemur, Cheirogaleus medius. Behav Ecol Sociobiol 49:8–17
Foerster K, Delhey K, Johnsen A, Lifjeld JT (2003) Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:715–717
Frasier TR (2008) STORM: software for testing hypotheses of relatedness and mating patterns. Mol Ecol Resour 8:1263–1266
Fridolfsson A-K, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30:116–121
Green AJ (2001) Mass/length residuals: measures of body condition or generations of spurious results? Ecology 82:1473–1483
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
Hayes JP, Shonkwiler JS (2001) Morphological indicators of body condition: useful or wishful thinking? In: Speakman JR (ed) Body composition analysis of animals: a handbook of non-destructive methods. Cambridge University Press, Cambridge, pp 8–38
Højsgaard S, Halekoh U, Yan J (2005) The R package geepack for generalized estimating equations. J Stat Softw 15:1–11
Huyvaert KP, Parker PG (2010) Extra-pair paternity in waved albatrosses: genetic relationships among females, social mates and genetic sires. Behaviour 147:1591–1613
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) Mate opportunity hypothesis and extrapair paternity in waved albatross (Phoebastria irrorata). Auk 123:524–536
Inchausti P, Weimerskirch H (2002) Dispersal and metapopulation dynamics of an oceanic seabird, the wandering albatross, and its consequences for its response to long-line fisheries. J Anim Ecol 71:765–770
Jones MGW (2011) Individual variation in reproductive success in the wandering albatross. Ph.D. thesis. Percy FitzPatrick Institute of African Ornithology, University of Cape Town, South Africa
Jouventin P, Lequette B, Dobson S (1999) Age-related mate choice in the wandering albatross. Anim Behav 57:1099–1106
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 149:67–78
Kempenaers B, Verheyen GR, Van den Broeck M, Burke T, Van Broeckhoven C, Dhondt AA (1992) Extra-pair paternity results from female preference for high-quality males in the blue tit. Nature 357:494–496
Li CC, Weeks DE, Chakravarti A (1993) Similarity of DNA fingerprints due to chance and relatedness. Hum Hered 43:45–52
Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655
Mauck RA, Marschall EA, Parker PG (1999) Adult survival and imperfect assessment of parentage: effects on male parenting decisions. Am Nat 154:99–109
Møller AP (2000) Male parental care, female reproductive success, and extra pair paternity. Behav Ecol 11:161–168
Møller AP, Birkhead TR (1993) Certainty of paternity covaries with paternal care in birds. Behav Ecol Sociobiol 33:261–268
Møller AP, Brohede J, Cuervo JJ, de Lope F, Primmer C (2003) Extrapair paternity in relation to sexual ornamentation, arrival date, and condition in a migratory bird. Behav Ecol 14:707–712
Munshi-South J (2007) Extra-pair paternity and the evolution of testis size in a behaviorally monogamous tropical mammal, the large treeshrew (Tupaia tana). Behav Ecol Sociobiol 62:210–212
Newton I (1989) Lifetime reproduction in birds. Academic, London
Petrie M, Kempenaers B (1998) Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol Evol 13:52–58
Prince PA, Ricketts C (1981) Relationships between food supply and growth in albatrosses: an interspecific chick fostering experiment. Ornis Scand 12:207–210
Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275
Reynolds JD, Colwell MA, Cooke F (1986) Sexual selection and spring arrival times of red-necked and Wilson's phalaropes. Behav Ecol Sociobiol 18:303–310
Ricketts C, Prince PA (1981) Comparison of growth of albatrosses. Ornis Scand 12:120–124
Ricklefs RE (1973) Patterns of growth in birds. II. Growth rate and mode of development. Ibis 115:177–210
Rios-Cardenas O, Webster MS (2005) Paternity and paternal effort in the pumpkinseed sunfish. Behav Ecol 16:914–921
Ryan PG, Phillips RA, Nel DC, Wood AG (2007) Breeding frequency in grey-headed albatrosses Thalassarche chrysostoma. Ibis 149:45–52
Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163
Stutchbury BJM (1998) Female mate choice of extra-pair males: breeding synchrony is important. Behav Ecol Sociobiol 43:213–215
Tickell WLN (1968) Biology of the great albatrosses, Diomedea exulans and Diomedea epomophora. Antarct Res Ser 12:1–55
Tickell WLN (2000) Albatrosses. Pica, Sussex
Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited Review. Mol Ecol 9:1013–1027
van de Casteele T, Galbusera P, Matthysen E (2001) A comparison of microsatellite based pairwise relatedness estimators. Mol Ecol 10:1539–1549
Weimerskirch H (1995) Regulation of foraging trips and incubation routine in male and female wandering albatrosses. Oecologia 102:37–43
Weimerskirch H, Lequette B, Jouventin P (1989) Development and maturation of plumage in the wandering albatross Diomedea exulans. J Zool 219:411–421
Weimerskirch H, Barbraud C, Lys P (2000) Sex differences in parental investment and chick growth in wandering albatross: fitness consequences. Ecology 81:309–318
Weimerskirch H, Lallemand J, Martin J (2005) Population sex ratio variation in a monogamous long-lived bird, the wandering albatross. J Anim Ecol 74:285–291
Westneat DF, Sargent RC (1996) Sex and parenting: the effect of sexual conflict and parentage on parental strategies. Trends Ecol Evol 11:87–91
Westneat DF, Sherman PW, Morton ML (1990) The ecology and evolution of extra-pair copulations in birds. Curr Ornithol 7:331–369
Wink M, Dyrcz A (1999) Mating systems in birds: a review of molecular studies. Acta Ornithol 34:91–104
Yan J (2002) geepack: yet another package for generalized estimating equations. R-News 2(3):12–14
Yan J, Fine JP (2004) Estimating equations for association structures. Stat Med 23:859–880
Young LC, Zaun BJ, VanderWerf EA (2008) Successful same-sex pairing in Laysan albatross. Biol Lett 4:323–325
Zeh JA, Zeh DW (1996) The evolution of polyandry I: intragenomic conflict and genetic incompatibility. Proc R Soc Lond B 263:1711–1717
Zeh JA, Zeh DW (2003) Toward a new sexual selection paradigm: polyandry, conflict and incompatibility. Ethology 109:929–950
Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, Berlin
Acknowledgements
Thanks to Quentin Hagens for valuable advice and assistance in formative stages of fieldwork. Henk Louw, Edith Mertz and Paul Visser gave extensive assistance with fieldwork. Some data are from long-term monitoring of wandering albatrosses at Marion Island, which was initiated by John Cooper. Some genetic analyses were performed at the DNA Sequencing Unit, Central Analytical Facility, Stellenbosch University. We thank two reviewers for their thoughtful comments on an earlier draft of this paper. Financial and logistical support was provided by the DST/NRF Centre of Excellence (CoE) at the Percy FitzPatrick Institute of African Ornithology and the South African National Antarctic Programme (through the National Research Foundation).
Ethical standards
Research conducted was approved by University of Cape Town’s Animal Ethics Committee and the Prince Edward Islands’ Management Committee. The authors declare that they have no conflict of interests.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by C. R. Brown
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 13.8 kb)
Rights and permissions
About this article
Cite this article
Jones, M.G.W., Techow, N.M.S.M. & Ryan, P.G. Dalliances and doubtful dads: what determines extra-pair paternity in socially monogamous wandering albatrosses?. Behav Ecol Sociobiol 66, 1213–1224 (2012). https://doi.org/10.1007/s00265-012-1374-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-012-1374-8
Keywords
- Extra-pair paternity
- Forced copulation
- Genetic variability
- Mate choice
- Monogamy
- Parental investment