Molecular evidence of extra-pair paternity and intraspecific brood parasitism by the Magellanic Penguin (Spheniscus magellanicus)


Molecular studies have shown that, although most avian species are socially monogamous, they can exhibit different reproductive strategies, such as extra-pair paternity (EPP) and intraspecific brood parasitism (IBP). We investigated the genetic mating system of the Magellanic Penguin, Spheniscus magellanicus, a species that is reported to be monogamous, with little or no evidence of extra-pair paternity, high partner faithfulness over the years and intense biparental care. Thus, we proposed that if EPP does occur, the rate will be low and could be related to increased genetic diversity among offspring or the body condition of parents. As a consequence, we hypothesize that offspring from EPP will exhibit faster growth than non-EPP offspring, thus increasing their survival probability. In contrast to expectations, EPP was detected in 31% of the offspring and 48% of the nests had at least one extra-pair young. In addition, 6% of chicks were not the offspring of the putative mother or either member of the social pair, indicating evidence of IBP. However, we did not find a difference in genetic diversity between nests with or without EPP, nor did we find differences in parent body condition. Offspring from EPP showed slightly faster growth than non-EPP offspring, although this difference was not statistically significant. These results reveal a high rate of EPP and a low rate of IBP, both of which were previously unknown for this species. Our findings demonstrate that the Magellanic penguin has a more complex social mating system than previously thought.


Molekularer Nachweis von Fremdvaterschaft und innerartlichem Brutparasitismus bei Magellan-Pinguinen ( Spheniscus magellanicus )

Molekulare Studien haben gezeigt, dass, obwohl die meisten Vogelarten sozial monogam leben, sie dennoch verschiedene Reproduktionsstrategien verfolgen können, wie beispielsweise Vaterschaften außerhalb der Paarbindung (extra-pair paternity EPP) oder intraspezifischer Brutparasitismus (IBP). Wir untersuchten das genetische Paarungssystem von Magellan-Pinguinen Spheniscus magellanicus , eine Art, die als monogam gilt, mit wenigen Nachweisen von Fremdvaterschaften, hoher Partnertreue über Jahre hinweg und einer intensiven Brutpflege durch beide Elterntiere. Daher nahmen wir an, dass, wenn EPP auftritt, die Rate gering sein wird und zusammenhängen könnte mit einer erhöhten genetischen Diversität unter den Nachkommen oder der Körperkondition der Eltern. Folglich stellten wir die These auf, dass Nachkommen aus Fremdvaterschaften ein schnelleres Wachstum zeigen und damit ihre Überlebenswahrscheinlichkeit erhöhen. Im Gegensatz zu den Erwartungen wurden Fremdvaterschaften in 31% der Nachkommen nachgewiesen. In 48% der Nester befand sich mindestens ein Jungvogel mit fremdem Vater. Darüber hinaus waren 6% der Küken nicht die Nachkommen der mutmaßlichen Mutter oder von keinem der beiden Brutpartner, der Beleg für IBP. Wir konnten jedoch keinen Unterschied in der genetischen Diversität zwischen Nestern mit und ohne EPP finden, noch fanden wir Unterschiede in der elterlichen Körperkondition. Die Nachkommen aus Fremdvaterschaften zeigten ein etwas schnelleres Wachstum als der leibliche Nachwuchs, wobei der Unterschied statistisch nicht signifikant war. Die Ergebnisse belegen einen hohen Anteil an EPP und einen niedrigen IBP-Anteil. Beide Strategien waren zuvor bei dieser Art nicht bekannt. Unsere Studie zeigt, dass Magellan-Pinguine ein weitaus komplexeres soziales Paarungssystem haben als zuvor bekannt war.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 99

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4


  1. Akst EP, Boersma PD, Fleischer RC (2002) A comparison of genetic diversity between the Galápagos penguin and the Magellanic penguin. Conserv Genet 3:375–383

  2. Arct A, Drobniak SM, Podmokła E, Gustafson L, Cichoń M (2013) Benefits of extra-pair mating may depend on environmental conditions: an experimental study in the blue tit (Cyanistes caeruleus). Behav Ecol Sociobiol 67:1809–1815

  3. Arnold KE, Owens IPF (2002) Extra-pair paternity and egg dumping in birds: life history, parental care and the risk of retaliation. Proc R Soc B 269:1263–1269

  4. Barrionuevo M, Frere E (2017) An experimental approach to the brood reduction hypothesis in Magellanic penguins. J Avian Biol 48:1077–1086

  5. Bennison C, Hemmings N, Slate J, Birkhead T (2015) Long sperm fertilize more eggs in a bird. Proc R Soc B 282:20141897

  6. Bertellotti M, Tella JL, Godoy JA, Blanco G, Forero MG, Donázar JA, Ceballos O (2002) Determining sex of Magellanic Penguins using molecular procedures and discriminant functions. Waterbirds 25:479–484

  7. BirdLife International (2016) Spheniscus magellanicus. The IUCN Red List for birds. Downloaded from on 24 Sept 2016

  8. Boersma PD, Rebstock GA (2009) Foraging distance affects reproductive success in Magellanic penguins. Mar Ecol Prog Ser 375:263–275

  9. Boersma PD, Frere E, Kane O, Pozzi LM, Putz K, Rey AR, Rebstock GA, Simenone A, Smith J, Buren AV, Yorio P, Borboroglu PG (2013) Magellanic Penguin. In: Borboroglu PG, Boersma PD (eds) Penguins: natural history and conservation. University of Washington Press, Seattle, pp 233–263

  10. Brown CR (1984) Laying eggs in a neighbor’s nest: benefits and costs of colonial nesting in swallows. Science 224:518–519

  11. Brown M, Lawes M (2007) Colony size and nest density predict the likelihood of parasitism in the colonial Southern Red Bishop Euplectes orix – Diderick Cuckoo Chrysococcyx caprius system. Ibis 149:321–327

  12. Dantas GPM, Almeida VS, Maracini P, Serra SD, Chame M, Labarthe N, Kolesnikovas C, Siciliano S, Matias CAR, Moura JF, Campos SDE, Mader A, Serafini PP (2013) Evidence for northward extension of the winter range of Magellanic Penguins along the Brazilian coast. Mar Ornithol 41:195–197

  13. Dreiss AN, Silva N, Richard M, Moyen F, Thery M, Møller AP, Danchin E (2008) Condition-dependent genetic benefits of extrapair fertilization in female blue tits Cyanistes caeruleus. J Evol Biol 21:1814–1822

  14. Duda N, Chȩtnicki W, Waldeck P, Andersson M (2008) Multiple maternity in black-headed gull Larus ridibundus clutches as revealed by protein fingerprinting. J Avian Biol 39:116–119

  15. Eikenaar C, Bonier F, Martin P, Moore I (2013) High rates of extra-pair paternity in two equatorial populations of rufous-collared sparrow, Zonotrichia capensis. J Avian Biol 44:600–602

  16. Gibbons DW (1986) Brood parasitism and cooperative nesting in the moorhern, Gallinula chloropus. Behav Ecol Sociobiol 19:221–232

  17. Griffin AS, Sheldon BC, West SA (2005) Cooperative breeders adjust offspring sex ratios to produce helpful helpers. Am Nat 166:628–632

  18. Griffith SC (2010) The role of multiple mating and extra-pair paternity in creating and reinforcing boundaries between species in birds. Emu 110:1–9

  19. Griffith S, Owens I, Thuman K (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212

  20. Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075

  21. 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

  22. Hood LC (1996) Adrenocortical response to stress in incubating Magellanic penguins (Spheniscus magellanicus) and mate switching in Magellanic penguins at Punta Tombo, Argentina. University of Washington, Seattle

  23. Hunter F, Miller G, Davis L (1995) Mate switching and copulation behaviour in the Adelie penguin. Behavior 132:691–707

  24. Jennions M, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64

  25. Johnson LS, Thompson CF, Sakaluk SK, Neuhäuser M, Johnson BG, Soukup SS, Forsythe AJ, Masters BS (2009) Extra-pair young in house wren broods are more likely to be male than female. Proc R Soc B 276:2285–2289

  26. Jones O, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Res 10:551–555

  27. Jones AG, Small CM, Paczolt KA, Ratterman NL (2010) A practical guide to methods of parentage analysis. Mol Ecol Res 10:6–30

  28. Ju J, Yin J, Racey P, Zhang L, Li D, Wan D (2014) Extra-pair paternity in Varied Tits Poecile varius. Acta Ornithol 49:131–137

  29. Kempenaers B, Verheyen GR, Dhondi AA (1997) Extrapair paternity in the blue tit (Parus caeruleus): female choice, male characteristics, and offspring quality. Behav Ecol 8:481–492

  30. Kingma SA, Hall ML, Segelbacher G, Peters A (2009) Radical loss of an extreme extra-pair mating system. BMC Ecol 9:15

  31. Komdeur J, Serge D, Tinbergen J, Mateman C (1997) Extreme adaptive modification in sex ratio of the Seychelles warbler’s eggs. Nature 385:522–525

  32. Komdeur J, Magrath MJL, Krackow S (2002) Pre-ovulation control of hatchling sex ratio in the Seychelles warbler. Proc R Soc Lond B 269:1067–1072

  33. Leech D, Hartley I, Stewart I, Griffith S, Burke T (2001) No effect of parental quality or extrapair paternity on brood sex ratio in the blue tit (Parus caeruleus). Behav Ecol 12:674–680

  34. Lezalová-Pialková R (2011) Molecular evidence for extra-pair paternity and intraspecific brood parasitism in the black-headed gull. J Ornithol 152:291–295

  35. Lindstrom MJ, Bates DM (1990) Nonlinear mixed effects models for repeated measures data. Biometrics 46:673–687

  36. Lorentsen SH, Amundsen T, Anthonisen K, Lifjeld JT (2000) Molecular evidence for extrapair paternity and female-female pairs in a socially monogamous colonial seabird, the Antarctic petrel. Auk 117:1050–1055

  37. Lyon BE, Eadie JM (2008) Conspecific brood parasitism in birds: a life-history perspective. Annu Rev Ecol Evol Syst 39:343–346

  38. Lyon BE, Everding S (1996) High frequency of conspecific brood parasitism in a colonial waterbird, the Eared Grebe Podiceps nigricollis. J Avian Biol 27:238–244

  39. Marr AB, Arcese P, Hochachka WM, Reid JM, Keller LF (2006) Interactive effects of environmental stress and inbreeding on reproductive traits in a wild bird population. J Anim Ecol 75:1406–1415

  40. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

  41. Mayer C, Pasinelli G (2012) New support for an old hypothesis: density affects extra-pair paternity. Ecol Evol 3:694–705

  42. McLean I, Kayes S, Murie J (2000) Genetic monogamy mirrors social monogamy in the Fiordland Crested Penguin. N Z J 27:311–316

  43. Mitrus J, Mitrus C, Rutkowski R, Sikora M (2014) Extra-pair paternity in relation to age of the Red-breasted Flycatcher Ficedula parva males. Avian Biol Res 7:111–116

  44. Moreno J, Boto L, Fargallo JA, León A, Potti J (2000) Absence of extra-pair fertilisations in the Chinstrap Penguin Pygoscelis antarctica. J Avian Biol 4:580–583

  45. Olsson O, Bonnedahl J, Anker-Nilssen P (2001) Mate switching and copulation behaviour in King Penguins. J Avian Biol 32:139–145

  46. Petrie M, Kempenaers B (1998) Extra-pair paternity in birds: explaining variation between species and populations. TREE 13:52–58

  47. Petrie M, Moller AP (1991) Laying eggs in others’ nests: intraspecific brood parasitism in birds. TREE 6:315–320

  48. 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

  49. Pinheiro J, Bates D, DebRoy R, Sarkar D, R Core Team (2015) Linear and nonlinear mixed effects models. R package.version 3.1-121

  50. Quillfeldt P, Masello JF, Segelbacher G (2012) Extra-pair paternity in seabirds: a review and case study of Thin-billed Prions Pachyptila belcheri. J Ornithol 153:367–373

  51. R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna,

  52. Radford AN, Blakey JK (2000) Is variation in brood sex ratios adaptive in the great tit (Parus major)? Behav Ecol 11:294–298

  53. Saino N, Ellegren H, Møller AP (1999) No evidence for adjustment of sex allocation in relation to paternal ornamentation and paternity in barn swallows. Mol Ecol 8:399–406

  54. Sambrook J, Russel DW (2001) Molecular cloning, vol 3, 3rd edn. Cold Spring Harbor Laboratory Press, New York

  55. Schlosser JA, Garner TJ, Dubach JM, Mcelligott AG (2003) Characterization of microsatellite loci in Humboldt penguin (Spheniscus humboldti) and crossamplification in other penguin species. Mol Ecol Notes 3:62–64

  56. Schlosser JA, Dubach JM, Garner TWJ, Arraya B, Bernal B, Simeone A, Smith KA, Wallace RS (2009) Evidence for gene flow differs from observed dispersal patterns in the Humboldt penguin, Spheniscus humboldti. Conserv Genet 10:839–849

  57. Schwartz M, Boness D, Schaeff C (1999) Female-solicited extrapair matings in Humboldt penguins fail to produce extrapair fertilizations. Behav Ecol 10:242–250

  58. Sorenson LG (1992) Variable mating system of a sedentary tropical duck: the whitecheeked pintail (Anas bahamensis bahamensis). Auk 109:277–292

  59. Spottiswoode C, Moller AP (2004) Genetic similarity and hatching success in birds. Proc R Soc B 271:267–272

  60. St Clair C (1995) Unfit mothers? Maternal infanticide in royal penguins. Anim Behav 50:1177–1185

  61. Stokes DL, Boersma PD (2000) Nesting density and reproductive success in a colonial seabird, the Magellanic Penguin. Ecology 81:2878–2891

  62. Stutchbury BJM, Morton ES (1995) The effect of breeding synchrony on extra-pair mating systems in songbirds. Behaviour 132:675–690

  63. Thusius KJ, Dunn PO, Peterson KA, Whittingham LA (2001) Extra-pair paternity is influenced by breeding synchrony and density in the common yellowthroat. Behav Ecol 12:633–639

  64. Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90–92

  65. Tschirren B, Postma E, Rutstein AN, Griffith SC (2012) When mothers make sons sexy: maternal effects contribute to the increased sexual attractiveness of extra-pair offspring. Proc R Soc B 279:1233–1240

  66. Wagner EL, Lee EJ, Boersma PD (2013) Patterns of acceptance of artificial eggs and chicks by Magellanic penguins (Spheniscus magellanicus). J Ornithol 154:99–105

  67. Weatherhead PJ, Yezerinac SM (1998) Breeding synchrony and extra-pair mating in birds. Behav Ecol Sociobiol 43:217–219

  68. Webster MS, Reichart L (2005) Use of microsatellites for parentage and kinship analyses in animals. Mol Evol 395:222–238

  69. Westneat DF, Sherman PW (1997) Density and extra-pair fertilizations in birds: a comparative analysis. Behav Ecol Sociobiol 41:205–215

  70. Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: causes, correlates, and conflict. Ann Rev Ecol Evol Syst 34:365–396

  71. Whittingham L, Dunn PO (2000) Offspring sex ratios in tree swallows: females in better condition produce more sons. Mol Ecol 9:1123–1129

  72. Wink M, Dyrcz A (1999) Mating systems in birds: a review of molecular studies. Acta Ornithol 34:91–109

  73. Yom-Tov Y (2001) An update list and some comments on the occurence of intraspecific nest parastism in birds. Ibis 143:133–143

  74. Yom-Tov Y, Geffen E (2017) Conspecific brood parasitism among birds: the effects of phylogeny, mode of reproduction and geographic distribution. In: Soler M (ed) Avian brood parasitism. Fascinating life sciences. Springer, Cham, pp 95–103

  75. Yorio P, García-Borboroglu P, Potti J, Moreno J (2001) Breeding biology of Magellanic Penguins, Spheniscus magellanicus, at Golfo San Jorge, Patagonia. Argentina Mar Ornithol 29:75–79

  76. Zeh JA, Zeh DW (2001) Reproductive mode and the genetic benefits of polyandry. Anim Behav 61:1051–1063

Download references


We thank Erik Wild for his English language review and comments on the draft. We appreciate the improvements in English usage made by Peter Lowther through the Association of Field Ornithologists’ program of editorial assistance. We are grateful to the Frere team for helping with field work, and the Laboratory of Biodiversity and Molecular Evolution of UFMG for support with MEGABASE. This study was financed by the National Counsel of Technological and Scientific Development of Brazil (CNPq 482264/2012-8); Coordination for the improvement of higher Educational personal (CAPES) provided a fellowship to ACMM. We thank anonymous reviewers for their insightful comments on the previous draft of this manuscript.


This research was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (Grant CNPq 482264/2012-8) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior.

Author information

Correspondence to Gisele Pires de Mendonça Dantas.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by M. Wink.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (TXT 12 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Marasco, A.C.M., Morgante, J.S., Barrionuevo, M. et al. Molecular evidence of extra-pair paternity and intraspecific brood parasitism by the Magellanic Penguin (Spheniscus magellanicus). J Ornithol 161, 125–135 (2020) doi:10.1007/s10336-019-01720-4

Download citation


  • Microsatellites
  • Body condition
  • Sex ratio
  • Extra-pair copulation
  • Genetic diversity