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Behavioral Ecology and Sociobiology

, Volume 63, Issue 6, pp 911–922 | Cite as

Multiple paternity and offspring quality in tree swallows

  • Peter O. Dunn
  • Jan T. Lifjeld
  • Linda A. Whittingham
Original Paper

Abstract

There is mounting evidence in a variety of taxa that females increase offspring quality by mating with multiple males, often resulting in multiple paternity. In birds, however, few studies have explicitly examined the benefits of mating with several different males; instead, the focus has been on whether or not extra-pair mating occurs, and its adaptive significance remains controversial. We examined the hypothesis that offspring quality, particularly immune response (phytohaemagglutinin assay) and growth, increases with the number of sires in broods of socially monogamous tree swallows (Tachycineta bicolor). We found one of the highest known levels of multiple paternity in birds (84% of nests with two or more extra-pair young had at least two extra-pair sires). Among nests with extra-pair young, the number and diversity of sires continued to increase linearly with the number of extra-pair young, so there was no evidence that some males monopolized paternity at high levels of extra-pair fertilization. Indeed, the number of sires was actually greater than expected in large broods, suggesting that some females might be seeking more mates. We found no effect of the number of sires on nestling immune response or growth. In mixed paternity broods, the immune response of extra-pair young did not differ from that of their within-pair half-siblings. However, among all broods, nestlings had a stronger immune response in nests with at least one extra-pair nestling than in nests with all within-pair nestlings. These results are not consistent with a good genes benefit of extra-pair mating, but they do suggest that there are environmental effects associated with extra-pair mating that increase nestling immune response. These environmental effects could produce indirect genetic effects on sexual selection if they are heritable. The extraordinarily high number of sires in this species highlights a relatively unexplored source of sexual selection in birds.

Keywords

Extra-pair paternity Genetic benefits Immune response Genetic polyandry 

Notes

Acknowledgments

We thank Mary Stapleton and Stacy Valkenaar for assistance in the field and the staff at University of Wisconsin-Milwaukee (UWM) Field Station for logistic support. Bryan Neff helped with the simulation model, and Jeff Graves, Bart Kempenaers, Dustin Rubenstein, and an anonymous reviewer provided helpful comments on the manuscript. This study was approved by the Animal Care and Use Committee at UWM (protocol 99-00#19). The project was funded by the National Science Foundation (LAW and POD) and the Nansen Endowment (JTL). JTL was supported by a grant from the University of Oslo and the Research Council of Norway during a sabbatical stay at UWM.

References

  1. Amos W, Wilmer JW, Fullard K, Burg TM, Croxall JP, Bloch D, Coulson T (2001) The influence of parental relatedness on reproductive success. Proc R Soc Lond B 268:2021–2027CrossRefGoogle Scholar
  2. Arnqvist G, Kirkpatrick M (2005) The evolution of infidelity in socially monogamous passerines: the strength of direct and indirect selection on extra-pair copulation behavior in females. Am Nat 165:S26–S37PubMedCrossRefGoogle Scholar
  3. Baer B, Schmid-Hempel P (1999) Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 397:151–154CrossRefGoogle Scholar
  4. Bitton P-P, O’Brien EL, Dawson RD (2007) Plumage brightness and age predict extrapair fertilization success of male tree swallows, Tachycineta bicolor. Anim Behav 74:1777–1784CrossRefGoogle Scholar
  5. Boag PT, Ratcliffe LM (2000) Genetics of avian mating systems. In: Apollonio M, Festa-Bianchet M, Mainardi D (eds) Vertebrate mating systems. World Scientific, Singapore, pp 307–332Google Scholar
  6. Brookfield JFY (1996) A simple method for estimating the null allele frequency from heterozygote deficiency. Mol Ecol 5:453–455PubMedCrossRefGoogle Scholar
  7. Brown JL (1997) A theory of mate choice based on heterozygosity. Behav Ecol 8:60–65CrossRefGoogle Scholar
  8. Christe P, de Lope F, González G, Saino N, Møller AP (2001) The influence of environmental conditions on immune response, morphology and recapture probability of nestling house martins (Delichon urbica). Oecologia 126:333–338CrossRefGoogle Scholar
  9. Cohas A, Yoccoz NG, Allainé D (2007) Extra-pair paternity in alpine marmots, Marmota marmota: genetic quality and genetic diversity effects. Behav Ecol Sociobiol 61:1081–1092CrossRefGoogle Scholar
  10. Coltman DW, Pilkington JG, Smith JA, Pemberton JM (1999) Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evolution 53:1259–1267CrossRefGoogle Scholar
  11. Crowe SA, Kleven O, Delmore KE, Laskemoen T, Nocera JJ, Lifjeld JT, Robertson RJ (2009) Paternity assurance through frequent copulations in a wild passerine with intense sperm competition. Anim Behav 77:183–187Google Scholar
  12. DiBattista JD, Feldheim KA, Gruber SH, Hendry AP (2008) Are indirect genetic benefits associated with polyandry? Testing predictions in a natural population of lemon sharks. Mol Ecol 17:783–795PubMedCrossRefGoogle Scholar
  13. Dunn PO, Afton AD, Gloutney ML, Alisaukas RT (1999) Forced copulation results in few extrapair fertilizations in Ross’s and lesser snow geese. Anim Behav 57:1071–1081PubMedCrossRefGoogle Scholar
  14. Edler R, Friedl TWP (2008) Within-pair young are more immunocompetent than extrapair young in mixed-paternity broods of the red bishop. Anim Behav 75:391–401CrossRefGoogle Scholar
  15. Firman RC, Simmons LW (2008) Polyandry facilitates postcopulatory inbreeding avoidance in house mice. Evolution 62:603–611PubMedCrossRefGoogle Scholar
  16. Fisher DO, Double MC, Blomberg SP, Jennions MD, Cockburn A (2006) Post-mating sexual selection increases lifetime fitness of polyandrous females in the wild. Nature 444:89–92PubMedCrossRefGoogle Scholar
  17. Forstmeier W, Coltman DW, Birkhead TR (2004) Maternal effects influence the sexual behavior of sons and daughters in the zebra finch. Evolution 58:2574–2583PubMedGoogle Scholar
  18. Garant D, Dodson JJ, Bernatchez L (2005) Offspring genetic diversity increases fitness of female Atlantic salmon (Salmo salar). Behav Ecol Sociobiol 57:240–244CrossRefGoogle Scholar
  19. Garvin JC, Abroe B, Pedersen MC, Dunn PO, Whittingham LA (2006) Immune response of nestling warblers varies with extra-pair paternity and temperature. Mol Ecol 15:3833–3840PubMedCrossRefGoogle Scholar
  20. Gil D, Graves J, Hazon N, Wells A (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286:126–128PubMedCrossRefGoogle Scholar
  21. Goodnight KF, Queller DC (1999) Computer software for performing likelihood tests of pedigree relationship using genetic markers. Mol Ecol 8:1231–1234CrossRefGoogle Scholar
  22. Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
  23. Griffith SC (2007) The evolution of infidelity in socially monogamous passerines: neglected components of direct and indirect selection. Am Nat 169:274–281PubMedCrossRefGoogle Scholar
  24. Griffiths R, Double M, Orr K, Dawson R (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1076PubMedCrossRefGoogle Scholar
  25. Groothuis TG, Eising CM, Dijkstra C, Müller W (2005) Balancing between costs and benefits of maternal hormone deposition in avian eggs. Biol Letters 1:78–81CrossRefGoogle Scholar
  26. Hoffman JI, Forcada J, Trathan PN, Amos W (2007) Female fur seals show active choice for males that are heterozygous and unrelated. Nature 445:912–914PubMedCrossRefGoogle Scholar
  27. Hoogland JL (1998) Why do female Gunnison’s prairie dogs copulate with more than one male? Anim Behav 55:351–359PubMedCrossRefGoogle Scholar
  28. Hopper KR, Rosenheim JA, Prout T, Oppenheim SJ (2003) Within-generation bet hedging: a seductive explanation? Oikos 101:219–222CrossRefGoogle Scholar
  29. Hussell D (1983) Age and plumage color in female tree swallows. J Field Ornithol 54:312–318Google Scholar
  30. Jamieson A (1994) The effectiveness of using co-dominant polymorphic allelic series for (1) checking pedigrees and (2) distinguishing full-sib pair members. Anim Gen 25:37–44Google Scholar
  31. Jeffreys AJ, Allen M, Hagelberg E, Sonnberg A (1992) Identification of the skeletal remains of Josef Mengele by DNA analysis. Forensic Sci Int 56:65–76PubMedCrossRefGoogle Scholar
  32. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64PubMedCrossRefGoogle Scholar
  33. Johnsen A, Andersen V, Sunding C, Lifjeld JT (2000) Female bluethroats enhance offspring immunocompetence through extra-pair copulations. Nature 406:296–299PubMedCrossRefGoogle Scholar
  34. Lane JE, Boutin S, Gunn MR, Slate J, Coltman DW (2008) Female multiple mating and paternity in free-ranging North American red squirrels. Anim Behav 75:1927–1937CrossRefGoogle Scholar
  35. Lee PLM, Hays GC (2004) Polyandry in a marine turtle: females make the best of a bad job. Proc Nat Acad Sci USA 101:6530–6535PubMedCrossRefGoogle Scholar
  36. Lifjeld J, Robertson R (1992) Female control of extra-pair fertilizations in tree swallows. Behav Ecol Sociobiol 31:89–96CrossRefGoogle Scholar
  37. Lifjeld JT, Dunn PO, Whittingham LA (2002) Short-term fluctuations in cellular immunity of tree swallows feeding nestlings. Oecologia 130:185–190Google Scholar
  38. Lochmiller RL, Vestey MR, Boren JC (1993) Relationship between protein nutritional status and immunocompetence in northern bobwhite chicks. Auk 110:503–510Google Scholar
  39. Madsen T, Shine R, Loman J, Hakansson T (1992) Why do female adders copulate so frequently? Nature 355:440–441CrossRefGoogle Scholar
  40. Mäkinen T, Panova M, André C (2007) High levels of multiple paternity in Littorina saxatilis: hedging the bets? J Hered 98:705–711PubMedCrossRefGoogle Scholar
  41. Maklakov AA, Lubin Y (2004) Sexual conflict over mating in a spider: increased fecundity does not compensate for the costs of polyandry. Evolution 58:1135–1140PubMedGoogle Scholar
  42. Martin LB, Han P, Lewittes J, Kuhlman JR, Klasing KC, Wikelski M (2006) Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Func Ecol 20:290–299CrossRefGoogle Scholar
  43. McCarty JP (2001) Varation in growth of nestling tree swallows across multiple temporal and spatial scales. Auk 118:176–190CrossRefGoogle Scholar
  44. McKinney F, Evarts S (1998) Sexual coercion in waterfowl and other birds. In: Parker P, Burley N (eds) Avian reproductive tactics: female and male perspectives, vol 49. American Ornithologists’ Union, Washington, D.C., pp 163–195Google Scholar
  45. Meek SB, Robertson RJ, Boag PT (1994) Extrapair paternity and intraspecific brood parasitism in eastern bluebirds revealed by DNA fingerprinting. Auk 111:739–744Google Scholar
  46. Mitton JB, Schuster WSF, Cothran EG, DeFries JC (1993) Correlation between the individual heterozygosity of parents and their offspring. Heredity 71:59–63PubMedCrossRefGoogle Scholar
  47. Navara KJ, Hill GE, Mendona MT (2006) Yolk androgen deposition as a compensatory strategy. Behav Ecol Sociobiol 60:392–398CrossRefGoogle Scholar
  48. Neff BD, Pitcher TE, Ramnarine IW (2008) Inter-population variation in multiple paternity and reproductive skew in the guppy. Mol Ecol 17:2975–2984PubMedCrossRefGoogle Scholar
  49. O’Brien EL, Dawson RD (2007) Context-dependent genetic benefits of extra-pair mate choice in a socially monogamous passerine. Behav Ecol Sociobiol 61:775–782CrossRefGoogle Scholar
  50. Olsson M, Gullberg A, Tegelström H, Madsen T, Shine R (1994) Can female adders multiply? Nature 369:528CrossRefGoogle Scholar
  51. Otter K, Ratcliffe L, Boag PT (1998) Do female black-capped chickadees prefer high-ranking males as extra-pair partners? Behav Ecol Sociobiol 43:25–36CrossRefGoogle Scholar
  52. Parker G (1990) Sperm competition games: raffles and roles. Proc R Soc Lond B 242:120–126CrossRefGoogle Scholar
  53. Petit R, el Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855CrossRefGoogle Scholar
  54. Poirier NE, Whittingham LA, Dunn PO (2004) Males achieve greater reproductive success through multiple broods than through extrapair mating in house wrens. Anim Behav 67:1109–1116CrossRefGoogle Scholar
  55. Richardson DS, Jury FL, Dawson DA, Salgueiro P, Komdeur J, Burke T (2000) Fifty Seychelles warbler (Acrocephalus sechellensis) microsatellite loci polymorphic in Sylviidae species and their cross-species amplification in other passerine birds. Mol Ecol 9:2225–2229CrossRefGoogle Scholar
  56. Robertson RJ, Rendell WB (2001) A long-term study of reproductive performance in tree swallows: the influence of age and senescence on output. J Anim Ecol 70:1014–1031CrossRefGoogle Scholar
  57. Robertson RJ, Stutchbury BJ, Cohen RR (1992) Tree Swallow. In: Poole A, Stettenheim P, Gill F (eds) The Birds of North America, no 11. Academy of Natural Sciences, Philadelphia, pp 1–28Google Scholar
  58. SAS Institute (2003) JMP 5.0.1 User’s guide. SAS Institute, Cary, NCGoogle Scholar
  59. Schmoll T, Dietrich V, Winkel W, Epplen JT, Schurr F, Lubjuhn T (2005) Paternal genetic effects on offspring fitness are context dependent within the extrapair mating system of a socially monogamous passerine. Evolution 59:645–657PubMedGoogle Scholar
  60. Schmoll T, Schurr FM, Winkel W, Epplen JT, Lubjuhn T (2007) Polyandry in coal tits Parus ater: fitness consequences of putting eggs into multiple genetic baskets. J Evol Biol 20:1115–1125PubMedCrossRefGoogle Scholar
  61. Simmons LW (2005) The evolution of polyandry: sperm competition, sperm selection and offspring viability. Ann Rev Ecol Evol Syst 36:125–146CrossRefGoogle Scholar
  62. Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohemagglutinin skin testing technique in studies of avian immunocompetence. Func Ecol 13:567–572CrossRefGoogle Scholar
  63. Sprenger D, Anthes N, Michiels N (2008) Multiple mating affects offspring size in the opisthobranch Chelidonura sandrana. Mar Biol 153:891–897CrossRefGoogle Scholar
  64. Stapleton M, Kleven O, Lifjeld J, Robertson R (2007) Female tree swallows (Tachycineta bicolor) increase offspring heterozygosity through extrapair mating. Behav Ecol Sociobiol 61:1725–1733CrossRefGoogle Scholar
  65. Tregenza T, Wedell N (1998) Benefits of multiple mates in the cricket Gryllus bimaculatus. Evolution 52:1726–1730CrossRefGoogle Scholar
  66. Tregenza T, Wedell N, Hosken DJ, Ward PI (2003) Maternal effects on offspring depend on female mating pattern and offspring environment in yellow dung flies. Evolution 57:297–304PubMedGoogle Scholar
  67. Venier LA, Robertson RJ (1991) Copulation behaviour of the tree swallow, Tachycineta bicolor: paternity assurance in the presence of sperm competition. Anim Behav 42:939–948CrossRefGoogle Scholar
  68. Venier LA, Dunn PO, Lifjeld JT, Robertson RJ (1993) Behavioural patterns of extra-pair copulation in tree swallows. Anim Behav 45:412–415CrossRefGoogle Scholar
  69. Whitlock MC, Schluter D (2009) The analysis of biological data. Roberts , Greenwood VillageGoogle Scholar
  70. Whittingham L, Dunn P (2000) Offspring sex ratios in tree swallows: females in better condition produce more sons. Mol Ecol 9:1123–1129PubMedCrossRefGoogle Scholar
  71. Whittingham LA, Dunn PO, Stapleton MK (2006) Repeatability of extra-pair mating in tree swallows. Mol Ecol 15:841–849PubMedCrossRefGoogle Scholar
  72. Whittingham LA, Dunn PO, Lifjeld JT (2007) Egg mass influences nestling quality in tree swallows, but there is no differential allocation in relation to laying order or sex. Condor 109:585–594CrossRefGoogle Scholar
  73. Yasui Y (1998) The ‘genetic benefits’ of female multiple mating reconsidered. Trends Ecol Evol 13:246CrossRefGoogle Scholar
  74. Yasui Y (2001) Female multiple mating as a genetic bet-hedging strategy when mate choice criteria are unreliable. Ecol Res 16:605–616CrossRefGoogle Scholar
  75. Zach R (1982) Hatching asychrony, egg size, growth, and fledging in tree swallows. Auk 99:695–700Google Scholar
  76. Zeh JA, Zeh DW (1996) The evolution of polyandry I: intragenomic conlict and genetic incompatibility. Proc R Soc Lond B 263:1711–1717CrossRefGoogle Scholar
  77. Zeh JA, Zeh DW (2006) Outbred embryos rescue inbred half-siblings in mixed-paternity broods of live-bearing females. Nature 439:201–203PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Peter O. Dunn
    • 1
  • Jan T. Lifjeld
    • 2
  • Linda A. Whittingham
    • 1
  1. 1.Department of Biological SciencesUniversity of Wisconsin-MilwaukeeMilwaukeeUSA
  2. 2.National Centre for Biosystematics, Natural History MuseumUniversity of OsloBlindernOsloNorway

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