Extra-pair paternity in socially monogamous Streaked Shearwaters: forced copulation or female solicitation?

Abstract

Seabirds are long-lived birds that invest in offspring at very high levels, for which male parental care is indispensable. These characteristics are thought to explain seabirds’ generally low level of extra-pair paternity (EPP). Although the Streaked Shearwater (Calonectris leucomelas) is a socially monogamous seabird, it is known to copulate outside its social pair bond, which implies the frequent occurrence of EPP. In the closely related Cory’s Shearwater Calonectris borealis, cuckoldry is related to body size of the social male. To determine whether body-size-related EPP occurs among Streaked Shearwaters, we established 39 new microsatellite markers for parentage analysis and compared body size between cuckolded and non-cuckolded males. With the new markers, we found that extra-pair males sired 17 (15.0%) of 113 offspring during the 2014–2016 study period, which included three 1.5-month chick-rearing periods. This percentage is among the highest recorded for seabirds. We also found the bill and wing length of cuckolded males to be significantly shorter than those of non-cuckolded males, and that females can reject attempted copulations. These observations imply that EPP in this species is size related and involves female acceptance.

Zusammenfassung

Fremdvaterschaft bei sozial monogamen Weißgesicht-Sturmtauchern: erzwungene Kopulation oder weibliche Aufforderung?

Seevögel gehören zu den langlebigen Vogelarten, welche in hohem Maße in ihre Nachkommen investieren, was eine väterliche Fürsorge unerlässlich macht. Diese Eigenschaften sollen den generell geringen Grad an Fremdvaterschaften (engl. extra-pair paternity, EPP) bei diesen Vögeln erklären. Obwohl der Weißgesicht-Sturmtaucher (Calonectris leucomelas) zu den sozial monogamen Seevögeln gehört, sind bei dieser Art Kopulationen außerhalb des sozialen Paarbundes bekannt, was ein häufiges Auftreten von EPP nahelegt. Beim nahverwandten Gelbschnabel-Sturmtaucher Calonectris borealis hängt das Fremdgehen mit der Körpergröße des sozialen Männchens zusammen. Um festzustellen, ob eine körpergrößenbezogene EPP beim Weißgesicht-Sturmtaucher vorkommt, haben wir 39 neue Mikrosatellitenmarker für die Vaterschaftsanalyse etabliert und die Körpergröße zwischen „betrogenen“und „nicht betrogenen“Männchen verglichen. Mit den neuen Markern konnten wir zeigen, dass Männchen außerhalb des Paarbundes 17 (15,0%) von 113 Nachkommen während des Untersuchungszeitraumes 2014-2016 zeugten. Der Untersuchungszeitraum umfasste drei Jungaufzuchten von jeweils 1,5 Monaten. Dieser prozentuale Anteil gehört zu den größten, die bislang bei Seevögeln ermittelt wurden. Weiterhin haben wir festgestellt, dass Schnabel- und Flügellänge der „betrogenen“Männchen signifikant kürzer als bei den „nicht betrogenen“Männchen waren. Zudem zeigte sich, dass Weibchen Kopulationsversuche abwehren können. Unsere Beobachtungen lassen bei dieser Art eine größenbezogene EPP vermuten, bei der die Akzeptanz des Weibchens erforderlich ist.

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

Fig. 1
Fig. 2

[Data for other birds were extracted from Table S15 in Cornwallis et al. (2010). Data for seabirds were extracted from Table 1 in Quillfeldt et al. (2011) and Table S15 in Cornwallis et al. (2010)]

References

  1. Andrew D, Douglas R, Sean LCO, Terry B (1994) Parental investment inversely related to degree of extra-pair paternity in the Reed Bunting. Nature 371:698–700

    Article  Google Scholar 

  2. Arima H, Sugawa H (2004) Correlation between the pitch of calls and external measurements of Streaked Shearwaters Calonectris leucomelas breeding on Kanmuri Island. Jpn J Ornithol 53:40–44

    Article  Google Scholar 

  3. Arima H, Oka N, Baba Y, Sugawa H, Ota T (2014) Gender identification by calls and body size of the Streaked Shearwater examined by CHD genes. Ornithol Sci 13:9–17

    Article  Google Scholar 

  4. Blacket MJ, Robin C, Good RT, Lee SF, Miller AD (2012) Universal primers for fluorescent labelling of PCR fragments—an efficient and cost-effective approach to genotyping by fluorescence. Mol Ecol Resour 12:456–463

    Article  CAS  PubMed  Google Scholar 

  5. Botstein D, White RL, Skolnick M, Davis RW (1980) Construction of a genetic linkage map in man using restriction fragment length polymorphisms. Am J Hum Genet 32:314–331

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Bried J, Dubois MP, Jarne P, Jouventin P, Santos RS (2010) Does competition for nests affect genetic monogamy in Cory’s Shearwater Calonectris diomedea? J Avian Biol 41:407–418

    Article  Google Scholar 

  7. Cornwallis CK, West SA, Davis KE, Griffin AS (2010) Promiscuity and the evolutionary transition to complex societies. Nature 466:969–972

    Article  CAS  PubMed  Google Scholar 

  8. Einoder LD, Page B, Goldsworthy SD (2008) Sexual size dimorphism and assortative mating in the Short-tailed Shearwater Puffinus tenurostiris. Mar Ornithol 36:167–173

    Google Scholar 

  9. Forstmeier W, Nakagawa S, Griffith SC, Kempenaers B (2014) Female extra-pair mating: adaptation or genetic constraint? Trends Ecol Evol 29:456–464

    Article  PubMed  Google Scholar 

  10. Gilbert L, Burke T, Krupa A (1998) No evidence for extra-pair paternity in the Western Gull. Mol Ecol 7:1549–1552

    Article  Google Scholar 

  11. 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

    Article  CAS  PubMed  Google Scholar 

  12. Hoi-Leitner M, Hoi H, Romero-Pujante M, Valera F (1999) Female extra–pair behaviour and environmental quality in the Serin (Serinus serinus): a test of the ‘constrained female hypothesis’. Proc R Soc Lond B 266:1021–1026

    Article  Google Scholar 

  13. Hsu YH, Schroeder J, Winney I, Burke T, Nakagawa S (2015) Are extra-pair males different from cuckolded males? A case study and a meta-analytic examination. Mol Ecol 24:1558–1571

    Article  PubMed  Google Scholar 

  14. Hutchinson JMC, Griffith SC (2008) Extra-pair paternity in the Skylark Alauda arvensis. Ibis 150:90–97

    Article  Google Scholar 

  15. Jouventin P, Bried J (2001) The effect of mate choice on speciation in Snow Petrels. Anim Behav 62:123–132

    Article  Google Scholar 

  16. Jouventin P, Charmantier A, Dubois MP, Phillipe J, Bried J (2007) Extra-pair paternity in the strongly monogamous Wandering Albatross Diomedea exulans has no apparent benefits for females. Ibis 149:67–78

    Article  Google Scholar 

  17. Kempenaers B, Verheyen GR, Dhondt AA (1997) Extrapair paternity in the Blue Tit Parus caeruleus: female choice, male characteristics, and offspring quality. Behav Ecol 8:481–492

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  19. Nava CP, Kim SY, Magalhaes MC, Neves V (2014) Do Cory’s Shearwaters Calonectris borealis choose mates based on size? J Ornithol 155:869–875

    Article  Google Scholar 

  20. Navarro J, Kaliontzopoulou A, González-Solís J (2009) Sexual dimorphism in bill morphology and feeding ecology in Cory’s Shearwater (Calonectris diomedea). Zoology 112:128–138

    Article  PubMed  Google Scholar 

  21. Oka N (2004) The distribution of Streaked Shearwater colonies, with special attention to population size, area of sea where located and surface water temperature. J Yamashina Inst Orinthol 35:164–188

    Article  Google Scholar 

  22. Petrie M, Kempenaers B (1998) Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol Evol 13:52–57

    Article  CAS  PubMed  Google Scholar 

  23. Quillfeldt P, Schmoll T, Peter HU, Epplen JT, Lubjuhn T (2001) Genetic monogamy in Wilson’s Storm-petrel. Auk 118(1):242–248

    Article  Google Scholar 

  24. Quillfeldt P, Masello JF, Segelbacher G (2011) Extra-pair paternity in seabirds: a review and case study of Thin-billed Prions Pachyptila belcheri. J Ornithol 153:367–373

    Article  Google Scholar 

  25. 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

    Article  Google Scholar 

  26. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Article  Google Scholar 

  27. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  28. Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  Google Scholar 

  29. Shirai M, Niizuma Y, Tsuchiya K, Yamamoto M, Oka N (2013) Sexual size dimorphism in Streaked Shearwaters Calonectris leucomelas. Ornithol Sci 12:57–62

    Article  Google Scholar 

  30. 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

    Article  CAS  Google Scholar 

  31. Székely T, Reynolds JD, Figuerola J (2000) Sexual size dimorphism in shorebirds, gulls, and alcids: the influence of sexual and natural selection. Evolution 54:1404–1413

    Article  PubMed  Google Scholar 

  32. Takeshima H, Muto N, Sakai Y, Ishiguro N, Iguchi K, Ishikawa S, Nishida M (2017) Rapid and effective isolation of candidate sequences for development of microsatellite markers in 30 fish species by using kit-based target capture and multiplexed parallel sequencing. Conserv Genet Resour 9:479–490

    Article  Google Scholar 

  33. Trivers R (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man 1871–1971. Aldine, Chicago, pp 139–179

    Google Scholar 

  34. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  CAS  Google Scholar 

  35. Verboven N, Mateman AC (1997) Low frequency of extra-pair fertilizations in the Great Tit Parus major revealed by DNA fingerprinting. J Avian Biol 28:231–239

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

  38. Wojczulanis-Jakubas K, Drobniak SM, Jakubas D, Kulpińska-Chamera M, Chaste O (2018) Assortative mating patterns of multiple phenotypic traits in a long-lived seabird. Ibis 160:464–469

    Article  Google Scholar 

  39. Yamamoto T, Takahashi A, Oka N, Iida T, Katsumata N, Sato K, Trathan PN (2011) Foraging areas of Streaked Shearwaters in relation to seasonal changes in the marine environment of the northwestern Pacific: inter-colony and sex-related differences. Mar Ecol Prog Ser 424:191–204

    Article  Google Scholar 

  40. Yoshida N (1981) Climbing the trees-Streaked Shearwaters with interesting behavior (Kini noboruumidori–Kichoohmizunagidori). Yubun, Tokyo (in Japanese)

    Google Scholar 

Download references

Acknowledgments

We thank Yoshinari Yonehara, Yusuke Goto, Tatsuya Shiozaki, and Takanori Sugahara for assisting with fieldwork on Funakoshi-Ohshima Island. We are grateful to Aran Garrod, Bart Kempenaers, and an anonymous referee for insightful comments that improved the manuscript. This study was supported by grants from research fellowships of the Japan Society for the Promotion of Science for Young Scientists to Miho Sakao, Tohoku Ecosystem-Associated Marine Sciences, the Bio-logging Science Program of the University of Tokyo, National Geographic (Asia 45-16), Japan Science Technology Agency Core Research for Evolutional Science and Technology (JPMJCR1685), the Cooperative Program of the Atmosphere and Ocean Research Institute, the University of Tokyo, and the Japan Society for the Promotion of Science and OP under the Japan-UK Research Cooperative Program. The authors declare no conflict of interest.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Miho Sakao.

Ethics declarations

All procedures performed in this study involving animals were approved by the Animal Experimental Committee of the University of Tokyo and conducted in accordance with the Guidelines for the Care of Experimental Animals. This work was conducted with permission from the Ministry of the Environment and Agency for Cultural Affairs, Japan.

Additional information

Communicated by M. Wink.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 4 (MP4 29424 kb)

Supplementary material 5 (MP4 20865 kb)

Supplementary material 1 (PDF 146 kb)

Supplementary material 2 (PDF 47 kb)

a

Fig. S1 Presence (n = 8) and absence (n=28) of extra-pair chicks in relation to the social female’s bill length (a), head length (b), tarsus length (c), wing length (d), and bill depth (e). Box plots show the median value, range, 25th and 75th percentiles, and outliers. P- and U-values were obtained by Mann–Whitney U-test. Supplementary material 3 (EPS 600 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sakao, M., Takeshima, H., Inoue, K. et al. Extra-pair paternity in socially monogamous Streaked Shearwaters: forced copulation or female solicitation?. J Ornithol 160, 137–144 (2019). https://doi.org/10.1007/s10336-018-1587-3

Download citation

Keywords

  • Extra-pair copulation
  • Microsatellite
  • Pair bond
  • Parental care
  • Cuckoldry