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Extra-Pair Paternity in the Wood Warbler (Phylloscopus sibilatrix) in Central Russia

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Abstract

Extra-pair paternity is widespread in passerine birds. The number of extra-pair young (EPY) varies among different species and populations of the same species. We tested if it is a case for a small passerine bird with poly-territorial behaviour, the Wood Warbler (Phylloscopus sibilatrix). The results are based on the microsatellite analysis of seven loci and revealed a high level of EPY in Central Russia population of Wood Warbler (EPY in 41% of all nests, 16 of 39 nests; 25% of all young were EPY, 52 of 212 young). We did not find relationship between relatedness among mates in the pair and the presence of EPY. There was no difference in heterozygosity and body mass between EPY and within pair young (WPY). Possible causes of extra-pair paternity are discussed.

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REFERENCES

  1. Akçay, E. and Roughgarden, J., Extra-pair paternity in birds: review of the genetic benefits, Evol. Ecol. Res, 2007, vol. 9, pp. 855–868. https://repository.upenn.edu/biology_papers/12.

    Google Scholar 

  2. Albrecht, T., Kreisinger, J., and Piálek, J., The strength of direct selection against female promiscuity is associated with rates of extrapair fertilizations in socially monogamous songbirds, Am. Nat., 2006, vol. 167, pp. 739–744. https://doi.org/10.1086/502633

    Article  PubMed  Google Scholar 

  3. Arct, A., Drobniak, S.M., Podmokła, E., Gustafson, L., and Cichoń, M., Benefits of extra-pair mating may depend on environmental conditions-an experimental study in the blue tit (Cyanistes caeruleus), Behav. Ecol. Sociobiol., 2013, vol. 67, pp. 1809–1815. https://doi.org/10.1007/s00265-013-1588-4

    Article  PubMed  PubMed Central  Google Scholar 

  4. Arct, A., Drobniak, S.M., and Cichon, M., Genetic similarity between mates predicts extrapair paternity—a meta-analysis of bird studies, Behav. Ecol., 2015, vol. 26, pp. 959–968. https://doi.org/10.1093/beheco/arv004

    Article  Google Scholar 

  5. Bensch, S., Price, T., and Kohn, J., Isolation and characterization of microsatellite loci in a Phylloscopus warbler, Mol. Ecol., 1997, vol. 6, pp. 91–92. https://doi.org/10.1046/j.1365-294X.1997.00150.x

    Article  CAS  PubMed  Google Scholar 

  6. Brouwer, L., van de Pol., M., Aranzamendi, N.H., Bain, G., Baldassarre, D.T., Brooker, L.C., Brooker, M.G., Colombelli-Négrel, D., Enbody, E., Gielow, K., Hall, M.L., Johnson, A.E., Karubian, J., Kingma, S.A., Kleindorfer, S., Louter, M., Mulder, R.A., Peters, A., Pruett-Jones, S., Tarvin, K.A., Thrasher, D.J., Varian-Ramos, C.W., Webster, M.S., and Cockburn, A., Multiple hypotheses explain variation in extra-pair paternity at different levels in a single bird family, Mol. Ecol., 2017. https://doi.org/https://doi.org/10.1111/mec.14385

  7. Canal, D., Potti, J., and Davilla, J.A., Male phenotype predicts extra-pair paternity in pied flycatchers, Behavior, 2011, vol. 148, pp. 691–712. https://doi.org/10.1163/000579511X573917

    Article  Google Scholar 

  8. Cassey, P., Ewen, J.G., and Moller, A.P., Revised evidence for facultative sex ratio adjustment in birds: a correction, Proc. Biol. Sci., 2006, vol. 273, pp. 3129–3130. https://doi.org/10.1098/rspb.2006.3628

    Article  PubMed  PubMed Central  Google Scholar 

  9. Charmantier, A., Blondel, J., Perret, P., and Lambrechts, M.M., Do extra-pair paternities provide genetic benefits for female blue tits Parus caeruleus?, J. Avian. Biol., 2004, vol. 35, pp. 524–532. https://doi.org/10.2307/3677557

    Article  Google Scholar 

  10. Dawson, D.A., Hanotte, O., Greig, C., Stewart, I.R., and Burke, T., Polymorphic microsatellites in the blue tit Parus caeruleus and their cross-species utility in 20 songbird families, Mol. Ecol., 2000, vol. 9, pp. 1941–1944. https://doi.org/10.1046/j.1365-294x.2000.01094-14.x

    Article  CAS  PubMed  Google Scholar 

  11. Dreiss, A.N., Navarro, C., De Lope, F., and Moller, A.P., Effects of an immune challenge on multiple components of song display in barn swallows Hirundo rustica: implications for sexual selection, Ethology, 2008, vol. 114, pp. 955–964. https://doi.org/10.1111/J.1439-0310.2008.01546.X

    Article  Google Scholar 

  12. Edly-Wright, C., Schwagmeyer, P.L., Parker, P.G., and Mock, D.W., Genetic similarity of mates, offspring health and extrapair fertilization in house sparrows, Anim. Behav., 2007, vol. 73, pp. 367–378. https://doi.org/10.1016/j.anbehav.2006.08.008

    Article  Google Scholar 

  13. Ellegren, H., Gustafsson, L., and Sheldon, B.C., Sex ratio adjustment in relation to paternal attractiveness in a wild bird population, Proc. Natl. Acad. Sci. U. S. A., 1996, vol. 93, pp. 11723–11728. https://doi.org/10.1073/pnas.93.21.11723

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  14. Ewen, J.G., Cassey, P., and Moller, A.P., Facultative primary sex ratio variation: a lack of evidence in birds, Proc. R. Soc. London, Ser. B, 2004, vol. 271, pp. 1277–1282. https://doi.org/10.1098/rspb.2004.2735

    Article  Google Scholar 

  15. Foerster, K., Delhey, K., Johnsen, A., Lifjeld, J.T., and Kempenaers, B., Females increase offspring heterozygosity and fitness through extra-pair matings, Nature, 2003, vol. 425, pp. 714–717. https://doi.org/10.1038/nature01969

    Article  ADS  CAS  PubMed  Google Scholar 

  16. Forstmeier, W., Kempenaers, B., Meyer, A., and Leisler, B., A novel song parameter correlates with extra-pair paternity and reflects male longevity, Proc. R. Soc. London, Ser. B, 2014a, vol. 269, pp. 1479–1485. https://doi.org/10.1098/rspb.2002.2039

    Article  Google Scholar 

  17. Forstmeier, W., Nakagawa, S., Griffith, S.C., and Kempenaers, B., Female extra-pair mating: adaptation or genetic constraint?, Trends Ecol. Evol., 2014, vol. 29, pp. 456–464.

    Article  PubMed  Google Scholar 

  18. Fossøy, F., Johnsen, A., and Lifjeld, J.T., Multiple genetic benefits of female promiscuity in a socially monogamous passerine, Evolution (New York), 2007, vol. 62, pp. 145–156. https://doi.org/10.1111/j.1558-5646.2007.00284.x

    Article  PubMed  Google Scholar 

  19. Gelter, H.P. and Tegelstrom, H., High frequency of extra-pair paternity in Swedish pied flycatchers revealed by allozyme electrophoresis and DNA fingerprinting, Behav. Ecol. Sociobiol., 1992, vol. 31, pp. 1–7. https://doi.org/10.1007/BF00167810

    Article  Google Scholar 

  20. Gil, D., Slater, P.J.B., and Graves, J., Extra-pair paternity and song characteristics in the willow warbler Phylloscopus trochilus, J. Avian Biol., 2007, vol. 38, pp. 291–297. https://doi.org/10.1111/j.2007.0908-8857.03868.x

    Article  Google Scholar 

  21. Goretskaya, M.Ya. and Gavrilov, V.V., Abundance and spatial structure of the warbler (Phylloscopus sibilatrix) population at the Zvenigorod Biological Station of Moscow State University for 2000–2016, in Dinamika chislennosti ptits v nazemnykh landshaftakh (Dynamics of Bird Abundance in Terrestrial Landscapes), 2017, pp. 204–206.

  22. Griffith, S.C. and Immler, S., Female infidelity and genetic compatibility in birds: the role of the genetically loaded raffle in understanding the function of extra-pair paternity, J. Avian Biol., 2009, vol. 40, pp. 97–101. https://doi.org/10.1111/j.1600-048X.2009.04562.x

    Article  Google Scholar 

  23. Griffiths, R., Double, M.C., Orr, K., and Dawson, R.J.G., A DNA test to sex most birds, Mol. Ecol., 1998, vol. 7, pp. 1071–1075.

    Article  CAS  PubMed  Google Scholar 

  24. Griffith, S.C., Owens, I.P.F., and Thuman, K.A., Extra pair paternity in birds: a review of interspecific variation and adaptive function, Mol. Ecol., 2002, vol. 11, pp. 2195–2212. https://doi.org/10.1046/j.1365-294X.2002.01613.x

    Article  CAS  PubMed  Google Scholar 

  25. Griffith, S.C., Ornborg, J., Russell, A.F., Andersson, S., and Sheldon, B.C., Correlations between ultraviolet coloration, overwinter survival and offspring sex ratio in the blue tit, J. Evol. Biol., 2003, vol. 16, pp. 1045–1054. https://doi.org/10.1046/j.1420-9101.2003.00550.x

    Article  CAS  PubMed  Google Scholar 

  26. Gyllensten, U.B., Jakobsson, S., and Temrin, H., No evidence for illegitimate young in monogamous and polygynous warblers, Lett. Nat., 1990, vol. 346, pp. 183–187. https://doi.org/10.1038/343168a0

    Article  Google Scholar 

  27. Hasselquist, D., Bensch, S., and von Schantz, T., Correlation between male song repertoire, extra-pair paternity and offspring survival in the great reed warbler, Nature, 1996, vol. 381, pp. 229–232. https://doi.org/10.1038/381229a0

    Article  ADS  CAS  Google Scholar 

  28. Hsu, Y-H., Schroeder, J., Winney, I., Burke, T., and Nakagawa, S., Are extra-pair males different from cuckolded males? A case study and a meta-analytic examination, Mol. Ecol., 2015, vol. 24, pp. 1558–1571. https://doi.org/10.1111/mec.13124

    Article  PubMed  Google Scholar 

  29. Jennions, M.D. and Petrie, M., Why do females mate multiply? A review of the genetic benefits, Biol. Rev., 2000, vol. 75, pp. 21–64. https://doi.org/10.1017/S0006323199005423

    Article  CAS  PubMed  Google Scholar 

  30. Johnsen, A., Andersen, V., Sunding, C., and Lifjeld, J.T., Female bluethroats enhance offspring immunocompetence through extra-pair copulations, Nature, 2000, vol. 406, pp. 296–299. https://doi.org/10.1038/35018556

    Article  ADS  CAS  PubMed  Google Scholar 

  31. Jones, A.G., GERUD 2.0: a computer program foe the reconstruction of parental genotypes from half-sib progeny arrays with known or unknown parents, Mol. Ecol. Notes, 2005, vol. 5, pp. 708–711. https://doi.org/10.1111/j.1471-8286.2005.01029.x

    Article  CAS  Google Scholar 

  32. Keller, L.F. and Waller, D.M., Inbreeding effects in wild populations, Trends Ecol. Evol., 2002, vol. 17, pp. 230–241. https://doi.org/10.1016/S0169-5347(02)02489-8

    Article  Google Scholar 

  33. Kempenaers, B., Verheyen, G.R., and Dhondi, A.A., Extrapair paternity in the blue tit (Parus caeruleus)?: female choice, male characteristics, and offspring quality, Behav. Ecol., 1997, vol. 8, pp. 481–492. https://doi.org/10.1093/beheco/8.5.481

    Article  Google Scholar 

  34. Kleven, O. and Lifjeld, J.T., No evidence for increased offspring heterozygosity from extrapair mating in the reed bunting (Emberiza schoeniclus), Behav. Ecol., 2005, vol. 16, pp. 561–565. https://doi.org/10.1093/beheco/ari027

    Article  Google Scholar 

  35. Leder, E.H., Karaiskou, N., and Primmer, C.R., Seventy new microsatellites for the pied flycatcher, Ficedula hypoleuca and amplification in other passerine birds, Mol. Ecol. Resour., 2008, vol. 8, pp. 874–880. https://doi.org/10.1111/j.1755-0998.2008.02096.x

    Article  CAS  PubMed  Google Scholar 

  36. Magrath, M.J.L., Vedder, O., van der Velde, M., and Komdeur, J., Maternal effects contribute to the superior performance of extra-pair offspring, Curr. Biol., 2009, vol. 19, pp. 792–797. https://doi.org/10.1016/j.cub.2009.03.068

    Article  CAS  PubMed  Google Scholar 

  37. Møller, A.P. and Erritzøe, J., Climate, body condition and spleen size in bird, Oecologia, 2003, vol. 137, pp. 621–626. https://doi.org/10.1007/s00442-003-1378-1

    Article  ADS  PubMed  Google Scholar 

  38. Nakagawa, S., Schroeder, J., and Burke, T., Sugar -free extrapair mating: a comment on Arct et al, Behav. Ecol., 2015, vol. 26, pp. 971–972. https://doi.org/10.1093/BEHECO/ARV041

    Article  Google Scholar 

  39. Neff, B.D. and Pitcher, T.E., Genetic quality and sexual selection: an integrated framework for good genes and compatible genes, Mol. Ecol., 2005, vol. 14, pp. 19–38. https://doi.org/10.1111/j.1365-294X.2004.02395.x

    Article  CAS  PubMed  Google Scholar 

  40. Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M., and Shipley, P., Micro-checker: software for identifying and correcting genotyping errors in microsatellite data, Mol. Ecol. Notes, 2004, vol. 4, pp. 535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x

    Article  CAS  Google Scholar 

  41. Peakall, R. and Smouse, P.E., GENALEX 6: genetic analysis in excel. population genetic software for teaching and research, Mol. Ecol. Notes, 2006, vol. 6, pp. 288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x

    Article  Google Scholar 

  42. Peakall, R. and Smouse, P.E., GenAlEx 6.5: genetic analysis in excel. population genetic software for teaching and research-an update, Bioinformatics, 2012, vol. 28, pp. 2537–2539. https://doi.org/10.1093/bioinformatics/bts460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Petrie, M. and Kempenaers, B., Extra-pair paternity in birds: explaining variation between species and populations, Trends Ecol. Evol., 1998, vol. 13, pp. 52–58. https://doi.org/10.1016/S0169-5347(97)01232-9

    Article  CAS  PubMed  Google Scholar 

  44. Pinheiro, J., Bates, D., DebRoy, S., and Sarkar, D., R Core Team, Nlme: linear and nonlinear mixed effects models, R package version 3.1-137, 2018. https://CRAN.R-project.org/package=nlme.

  45. Pipoly, I., Bokony, V., Kirkpatrick, M., Donald, P.F., Szekely, T., and Liker, A., The genetic sex-determination system predicts adult sex ratios in tetrapods, Nature, 2015, vol. 527, pp. 91–94.

    Article  ADS  CAS  PubMed  Google Scholar 

  46. Primmer, C., Moller, A., and Ellegren, H., New microsatellites from the pied flycatcher Ficedula hypoleuca and the swallow Hirundo rustica genomes, Hereditas, 1996, vol. 124, pp. 281–284. https://doi.org/10.1038/nature15380

    Article  CAS  PubMed  Google Scholar 

  47. Queller, D.C. and Goodnight, K.F., Estimating relatedness using molecular markers, Evolution, 1989, vol. 43, pp. 258–275. https://doi.org/10.1111/j.1558-5646.1989.tb04226.x

    Article  PubMed  Google Scholar 

  48. R Core Team, R: A Language and Environment for Statistical Computing, Vienna, Austria: R Foundation for Statistical Computing, 2021. https://www.R-project.org/.

  49. Richardson, D.S., Jury, F.L., and Blaakmeer, K., Komdeurj., burket. parentage assignment and extra-group paternity in a cooperative breeder: the Seychelles warbler (Acrocephalus sechellensis), Mol. Ecol., 2001, vol. 10, pp. 2263–2273. https://doi.org/10.1046/j.0962-1083.2001.01355.x

    Article  CAS  PubMed  Google Scholar 

  50. Santos, E.S.A., Santos, L.L.S., Lagisz, M., and Nakagawa, S., Conflict and cooperation over sex: the consequences of social and genetic polyandry for reproductive success in dunnocks, J. Anim. Ecol., 2015, vol. 84, pp. 1509–1519. https://doi.org/10.1111/1365-2656.12432

    Article  PubMed  Google Scholar 

  51. Schlicht, L., Valcu, M., and Kempenaers, B., Male extraterritorial behaviour predicts extrapair paternity pattern in blue tits, Cyanistes caeruleus, Behav. Ecol., 2015, vol. 26, pp. 1404–1413.

    Article  Google Scholar 

  52. Sheldon, B.C., Merilo, J., Qvarnstrom, A., Gustafsson, L., and Ellegren, H., Paternal genetic contribution to offspring condition predicted by size of male secondary sexual character, Proc. R. Soc. London, Ser. B, 1997, vol. 264, pp. 297–302 https://doi.org/10.1098/rspb.1997.0042

    Article  ADS  Google Scholar 

  53. Strohbach, S., Curio, E., Bathen, A., Epplen, J.T., and Lubjuhn, T., Extra-pair paternity in the great tit (Parus major): a test of the “good genes” hypothesis, Behav. Ecol., 1998, vol. 9, pp. 388–396.

    Article  Google Scholar 

  54. Suter, S.M., Keiser, M., Feignoux, R., and Meyer, D.R., Reed bunting females increase fitness through extra-pair mating with genetically dissimilar males, Proc. R. Soc. London, Ser. B, 2007, vol. 274, pp. 2865–2871. https://doi.org/10.1098/rspb.2007.0799

    Article  Google Scholar 

  55. Temrin, H., Why are some wood warbler (Phylloscopus sibilatrix) males polyterritorial, Ann. Zool. Fenn., 1984, vol. 21, pp. 243–247.

    Google Scholar 

  56. Temrin, H., Brodin, A., Åkerström, O., and Stenius, S., Parental investment in monogamous pairs of wood warblers (Phylloscopus sibilatrix), J. Ornithol., 1997, vol. 138, pp. 93–101. https://doi.org/10.1007/BF01651655

    Article  Google Scholar 

  57. Tregenza, T. and Wedell, N., Genetic compatibility, mate choice and patterns of parentage: invited review, Mol. Ecol., 2000, vol. 9, pp. 1013–1027. https://doi.org/10.1046/j.1365-294x.2000.00964.x

    Article  CAS  PubMed  Google Scholar 

  58. Westerdahl, H., Bensch, S., Hansson, B., Hasselquist, D., and von Schantz, T., Brood sex ratios, female harem status and resources for nestling provisioning in the great reed warbler (Acrocephalus arundinaceus), Behav. Ecol. Sociobiol., 2000, vol. 47, pp. 312–318. https://doi.org/10.1007/s002650050671

    Article  Google Scholar 

  59. Zuur, A.F., Ieno, E.N., Walker, N.J., Saveliev, A.A., and Smith, G.M., Mixed Effects Models and Extensions in Ecology with R, Springer, 2009. https://doi.org/10.18637/jss.v032.b01

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ACKNOWLEDGMENTS

The authors are grateful to V.N. Moskalenko and all students and assistants who participated in the bird capturing and observations during student practice at the ZBS from 2010 to 2015.

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This work was supported by ongoing institutional funding. No additional grants to carry out or direct this particular research were obtained.

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  1. Zvenigorod Biological Station, Biological Faculty, Lomonosov Moscow State University, 119991, Moscow, Russia

    M. I. Goretskaia

  2. Vavilov Institute of General Genetics Russian Academy of Sciences, 119991, Moscow, Russia

    Y. S. Belokon & M. M. Belokon

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  1. M. I. Goretskaia
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Correspondence to M. I. Goretskaia.

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All procedures were performed in accordance with the legislation of the Russian Federation. The study was approved by the Committee of Bioethics of Lomonosov Moscow State University (protocol # 69_O dated June 9, 2016).

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Goretskaia, M.I., Belokon, Y.S. & Belokon, M.M. Extra-Pair Paternity in the Wood Warbler (Phylloscopus sibilatrix) in Central Russia. Biol Bull Russ Acad Sci 51, 152–158 (2024). https://doi.org/10.1134/S1062359023601489

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