Behavioral Ecology and Sociobiology

, Volume 61, Issue 11, pp 1725–1733 | Cite as

Female tree swallows (Tachycineta bicolor) increase offspring heterozygosity through extrapair mating

  • Mary K. Stapleton
  • Oddmund Kleven
  • Jan T. Lifjeld
  • Raleigh J. Robertson
Original Paper

Abstract

Recent attention has focused on genetic compatibility as an adaptive function for why females engage in extrapair mating. We tested the genetic compatibility hypothesis in tree swallows (Tachycineta bicolor) over five breeding seasons using data from ten microsatellite loci. Tree swallows are socially monogamous passerines exhibiting high levels of extrapair paternity. Overall, we found that 47% of offspring were the result of extrapair fertilizations, and 83% of females produced at least one extrapair offspring. Consistently for all years, extrapair offspring were more heterozygous than their maternal half-siblings, which is in accordance with the genetic compatibility hypothesis. The difference was largely caused by the high heterozygosity of extrapair offspring sired by unknown males, suggesting that females are engaging in extrapair copulations with geographically distant males to increase the likelihood of being inseminated by a more compatible mate. Our findings support the idea that postcopulatory mechanisms are important for females when assessing potential sires for their offspring.

Keywords

Tree swallows Genetic similarity Extrapair mating Extrapair paternity Tachycineta bicolor Heterozygosity Genetic compatibility Genetic diversity Microsatellites 

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 Biol Sci 268:2021–2027PubMedCrossRefGoogle Scholar
  2. Arnqvist G, Kirkpatrick M (2005) The evolution of infidelity in socially monogamous passerines: the strength of direct and indirect selection on extrapair copulation behavior in females. Am Nat 165:S26–S37PubMedCrossRefGoogle Scholar
  3. Balloux F, Amos W, Coulson T (2004) Does heterozygosity estimate inbreeding in real populations? Mol Ecol 13:3021–3031PubMedCrossRefGoogle Scholar
  4. Barber CA, Robertson RJ, Boag PT (1996) The high frequency of extra-pair paternity in tree swallows is not an artifact of nestboxes. Behav Ecol Sociobiol 38:425–430CrossRefGoogle Scholar
  5. Barber CA, Edwards MJ, Robertson RJ (2005) A test of the genetic compatibility hypothesis with tree swallows, Tachycineta bicolor. Can J Zool 83:955–961CrossRefGoogle Scholar
  6. Bensch S, Hasselquist D, Von Schantz T (1994) Genetic similarity between parents predicts hatching failure: nonincestuous inbreeding in the great reed warbler? Evolution 48:317–326CrossRefGoogle Scholar
  7. Bensch S, Price T, Kohn J (1997) Isolation and characterization of microsatellite loci in a Phylloscopus warbler. Mol Ecol 6:91–92PubMedCrossRefGoogle Scholar
  8. Birkhead TR (1998) Sperm competition in birds: mechanisms and function. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Cambridge University Press, CambridgeGoogle Scholar
  9. Birkhead TR, Brillard JP (2007) Reproductive isolation in birds: postcopulatory prezygotic barriers. Trends Ecol Evol 22:266–272PubMedCrossRefGoogle Scholar
  10. Birkhead TR, Møller AP (1998) Sperm competition and sexual selection. Academic, San Diego, CaliforniaGoogle Scholar
  11. Blomqvist D, Andersson M, Kuepper C, Cuthill IC, Kis J, Lanctot RB, Sandercock BK, Szekely T, Wallander J, Kempenaers B (2002) Genetic similarity between mates and extra-pair parentage in three species of shorebirds. Nature (Lond) 419:613–615CrossRefGoogle Scholar
  12. Brown JL (1997) A theory of mate choice based on heterozygosity. Behav Ecol 8:60–65CrossRefGoogle Scholar
  13. Brown JL (1998) The new heterozygosity theory of mate choice and the MHC. Genetica (Dordr) 104:215–221CrossRefGoogle Scholar
  14. Butler RW (1988) Population dynamics and migration routes of tree swallows Tachycineta bicolor in North America. J Field Ornithol 59:395–402Google Scholar
  15. Clark L (1991) Odor detection thresholds in tree swallows and cedar waxwings. Auk 108:177–180Google Scholar
  16. Colgrave N, Ruxton GD (2003) Confidence intervals are a more useful complement to nonsignificant tests than are power calculations. Behav Ecol 14:446–447CrossRefGoogle Scholar
  17. 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
  18. Conrad KF, Johnston PV, Crossman C, Kempenaers B, Robertson RJ, Wheelwright NT, Boag PT (2001) High levels of extra-pair paternity in an isolated, low-density, island population of tree swallows (Tachycineta bicolor). Mol Ecol 10:1301–1308PubMedCrossRefGoogle Scholar
  19. Coulson T, Albon S, Slate J, Pemberton J (1999) Microsatellite loci reveal sex-dependent responses to inbreeding and outbreeding in red deer calves. Evolution 53:1951–1960CrossRefGoogle Scholar
  20. Crossman C (1996) Single-locus DNA profiling in the tree swallow, Tachycineta bicolor: a comparison of methods. MSc, Queen’s University, KingstonGoogle Scholar
  21. Dawson DA, Hanotte O, Greig C, Stewart IRK, Burke T (2000) Polymorphic microsatellites in the blue tit Parus caeruleus and their cross-species utility in 20 songbird families. Mol Ecol 9:1941–1944PubMedCrossRefGoogle Scholar
  22. Dunn PO, Robertson RJ (1993) Extra-pair paternity in polygynous tree swallows. Anim Behav 45:231–239CrossRefGoogle Scholar
  23. Dunn PO, Whittingham LA (2005) Radio-tracking of female tree swallows prior to egg-laying. J Field Ornithol 76:259–263Google Scholar
  24. Dunn PO, Whittingham LA (2007) Search costs influence the spatial distribution, but not the level, of extra-pair mating in tree swallows. Behav Ecol Sociobiol 61:449–454CrossRefGoogle Scholar
  25. Dunn PO, Robertson RJ, Michaud-Freeman D, Boag PT (1994a) Extra-pair paternity in tree swallows: why do females mate with more than one male? Behav Ecol Sociobiol 35:273–281CrossRefGoogle Scholar
  26. Dunn PO, Whittingham LA, Lifjeld JT, Robertson RJ, Boag PT (1994b) Effects of breeding density, synchrony, and experience on extrapair paternity in tree swallows. Behav Ecol 5:123–129CrossRefGoogle Scholar
  27. Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton, New JerseyGoogle Scholar
  28. Fernando P, Evans BJ, Morales JC, Melnick DJ (2001) Electrophoresis artifacts—a previously unrecognized cause of error in microsatellite analysis. Mol Ecol Notes 1:325–328CrossRefGoogle Scholar
  29. Foerster K, Delhey K, Johnsen A, Lifjeld JT, Kempenaers B (2003) Females increase offspring heterozygosity and fitness through extra-pair matings. Nature (Lond) 425:714–717CrossRefGoogle Scholar
  30. Freeman-Gallant CR, Meguerdichian M, Wheelwright NT, Sollecito SV (2003) Social pairing and female mating fidelity predicted by restriction fragment length polymorphism similarity at the major histocompatibility complex in a songbird. Mol Ecol 12:3077–3083PubMedCrossRefGoogle Scholar
  31. Griffith SC, Stewart IRK, Dawson DA, Owens IPF, Burke T (1999) Contrasting levels of extra-pair paternity in mainland and island populations of the house sparrow (Passer domesticus): Is there an ‘island effect’? Biol J Linn Soc 68:303–316CrossRefGoogle Scholar
  32. Griffith SC, Owens IPF, Thuman KA (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212PubMedCrossRefGoogle Scholar
  33. Hansson B, Westerberg L (2002) On the correlation between heterozygosity and fitness in natural populations. Mol Ecol 11:2467–2474PubMedCrossRefGoogle Scholar
  34. Hansson B, Bensch S, Hasselquist D, Akesson M (2001) Microsatellite diversity predicts recruitment of sibling great reed warblers. Proc Biol Sci 268:1287–1291PubMedCrossRefGoogle Scholar
  35. Hussell DJT (1983) Age and plumage color in female tree swallows. J Field Ornithol 54:312–318Google Scholar
  36. Jamieson A (1994) The effectiveness of using co-dominant polymorphic allelic series for (1) checking pedigrees and (2) distinguishing full-sib pair members. Anim Genet 25:37–44PubMedGoogle Scholar
  37. Jeffreys AJ, Allen MJ, Hagelberg E, Sonnberg A (1992) Identification of the skeletal remains of Josef Mengele by DNA analysis. Forensic Sci Int 56:65–76PubMedCrossRefGoogle Scholar
  38. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev (Camb) 75:21–64CrossRefGoogle Scholar
  39. Jones RB, Roper TJ (1997) Olfaction in the domestic fowl: a critical review. Phys and Behav 62:1009–1018CrossRefGoogle Scholar
  40. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241CrossRefGoogle Scholar
  41. Kempenaers B, Lanctot RB, Robertson RJ (1998) Certainty of paternity and paternal investment in eastern bluebirds and tree swallows. Anim Behav 55:845–860PubMedCrossRefGoogle Scholar
  42. Kempenaers B, Congdon B, Boag P, Robertson RJ (1999) Extrapair paternity and egg hatchability in tree swallows: evidence for the genetic compatibility hypothesis? Behav Ecol 10:304–311CrossRefGoogle Scholar
  43. Kempenaers B, Everding S, Bishop C, Boag P, Robertson RJ (2001) Extra-pair paternity and the reproductive role of male floaters in the tree swallow (Tachycineta bicolor). Behav Ecol Sociobiol 49:251–259CrossRefGoogle Scholar
  44. Lifjeld JT, Robertson RJ (1992) Female control of extra-pair fertilization in tree swallows. Behav Ecol Sociobiol 31:89–96CrossRefGoogle Scholar
  45. Lifjeld JT, Dunn PO, Robertson RJ, Boag PT (1993) Extra-pair paternity in monogamous tree swallows. Anim Behav 45:213–229CrossRefGoogle Scholar
  46. Madsen T, Shine R, Loman J, Hakansson T (1992) Why do female adders copulate so frequently? Nature (Lond) 355:440–441CrossRefGoogle Scholar
  47. Mays HL Jr, Hill G (2004) Choosing mates: good genes versus genes that are a good fit. Trends Ecol Evol 19:554–559PubMedCrossRefGoogle Scholar
  48. McDonald DB, Potts WK (1994) Cooperative display and relatedness among males in a lek-mating bird. Science (Wash DC) 266:1030–1032CrossRefGoogle Scholar
  49. Miller SA, Dykes DD, Polesky HF (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16Google Scholar
  50. Møller AP (1992) Frequency of female copulations with multiple males and sexual selection. Am Nat 139:1089–1101CrossRefGoogle Scholar
  51. Neff BD, Pitcher TE (2005) Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol Ecol 14:19–38PubMedCrossRefGoogle Scholar
  52. Newcomer SD, Zeh JA, Zeh DW (1999) Genetic benefits enhance the reproductive success of polyandrous females. Proc Natl Acad Sci USA 96:10236–10241PubMedCrossRefGoogle Scholar
  53. Olsson M, Gullberg A, Tegelstrom H (1994) Sperm competition in the sand lizard, Lacerta agilis. Anim Behav 48:193–200CrossRefGoogle Scholar
  54. Otter K, Ratcliffe L, Michaud D, Boag PT (1998) Do female black-capped chickadees prefer high-ranking males as extra-pair partners? Behav Ecol Sociobiol 43:25–36CrossRefGoogle Scholar
  55. Penn DJ (2002) The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108:1–21CrossRefGoogle Scholar
  56. Primmer CR, Møller AP, Ellegren H (1995) Resolving genetic relationships with microsatellite markers: a parentage testing system for the swallow Hirundo rustica. Mol Ecol 4:493–498PubMedGoogle Scholar
  57. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275CrossRefGoogle Scholar
  58. 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
  59. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New YorkGoogle Scholar
  60. SAS Institute (2000), JMPIN, 4.0.3. SAS Institute, Minneapolis, MinnesotaGoogle Scholar
  61. Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90CrossRefGoogle Scholar
  62. Simmons LW, Stockley P, Jackson RL, Parker GA (1996) Sperm competition or sperm selection: no evidence for female influence over paternity in yellow dung flies Scatophaga stercoraria. Behav Ecol Sociobiol 38:199–206CrossRefGoogle Scholar
  63. Slate J, Kruuk LEB, Marshall TC, Pemberton JM, Clutton-Brock TH (2000) Inbreeding depression influences lifetime breeding success in a wild population of red deer (Cervus elaphus). Proc R Soc B 267:1657–1662PubMedCrossRefGoogle Scholar
  64. Slate J, David P, Dodds KG, Veenvliet BA, Glass BC, Broad TE, McEwan JC (2004) Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity 93:255–265PubMedCrossRefGoogle Scholar
  65. SPSS (2003), SPSS for Windows, Release 12. SPSS, ChicagoGoogle Scholar
  66. Stapleton M, Robertson RJ (2006) Female tree swallow home range movements during their fertile period revealed by radio-tracking. Wilson J Ornithol 118:502–507CrossRefGoogle Scholar
  67. StatSoft (2003), STATISTICA, 6th edition, StatSoftGoogle Scholar
  68. Stenzler LM (2001) Genetic population structure in two bird species with contrasting dispersal behavior: the tree swallow (Tachycineta bicolor) and the Florida scrub-jab (Aphelocoma coerulescens). MSc Thesis, Cornell University, Ithaca, New YorkGoogle Scholar
  69. Tarvin KA, Webster MS, Tuttle EM, Pruett-Jones S (2005) Genetic similarity of social mates predicts the level of extrapair paternity in splendid fairy-wrens. Anim Behav 70:945–955CrossRefGoogle Scholar
  70. Tregenza T, Wedell N (1998) Benefits of multiple mates in the cricket, Gryllus bimaculatus. Evolution 52:1726–1730CrossRefGoogle Scholar
  71. Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013–1027PubMedCrossRefGoogle Scholar
  72. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man 1871–1971. Aldine, Chicago, pp 136–179Google Scholar
  73. Venier LA, Dunn PO, Lifjeld JT, Robertson RJ (1993) Behavioural patterns of extra-pair copulation in tree swallows. Anim Behav 45:412–415CrossRefGoogle Scholar
  74. Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: causes, correlates, and conflict. Annu Rev Ecol Evol Syst 34:365–396CrossRefGoogle Scholar
  75. Whittingham LA, Dunn PO (2001) Survival of extrapair and within-pair young in tree swallows. Behav Ecol 12:496–500CrossRefGoogle Scholar
  76. Whittingham LA, Dunn PO, Stapleton MK (2006) Repeatability of extra-pair mating in tree swallows. Mol Ecol 15:841–849PubMedCrossRefGoogle Scholar
  77. Worthington Wilmer J, Allen PJ, Pomeroy PP, Twiss SD, Amos W (1999) Where have all the fathers gone? An extensive microsatellite analysis of paternity in the grey seal (Halichoerus grypus). Mol Ecol 8:1417–1429PubMedCrossRefGoogle Scholar
  78. Zeh JA (1997) Polyandry and enhanced reproductive success in the harlequin-beetle-riding pseudoscorpion. Behav Ecol Sociobiol 40:111–118CrossRefGoogle Scholar
  79. Zeh JA, Zeh DW (1996) The evolution of polyandry I: intragenomic conflict and genetic incompatibility. Proc R Soc Lond B Biol Sci 263:1711–1717CrossRefGoogle Scholar
  80. Zeh JA, Zeh DW (1997) The evolution of polyandry II: post-copulatory defences against genetic incompatibility. Proc R Soc Lond B Biol Sci 264:69–75CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Mary K. Stapleton
    • 1
  • Oddmund Kleven
    • 2
  • Jan T. Lifjeld
    • 2
  • Raleigh J. Robertson
    • 1
  1. 1.Department of BiologyQueen’s UniversityKingstonCanada
  2. 2.Department of Zoology, Natural History MuseumUniversity of OsloOsloNorway

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