Advertisement

Behavioral Ecology and Sociobiology

, Volume 67, Issue 2, pp 243–255 | Cite as

Positive association between social and extra-pair mating in a polygynous songbird, the dickcissel (Spiza americana)

  • Bridget F. SousaEmail author
  • David F. Westneat
Original Paper

Abstract

In polygynous species, males appear to gain additional offspring by pairing with multiple females simultaneously. However, this may not be true if some females copulate outside of the social pair bond. Polygynous males could experience lower paternity because of trade-offs among gaining multiple social mates, guarding fertility with these mates, and pursuing extra-pair matings. Alternatively, polygynous males could simultaneously gain extra social mates and have high paternity, either because of female preferences or because of male competitive attributes. We tested four predictions stemming from these hypotheses in a facultatively polygynous songbird, the dickcissel (Spiza americana). Unlike most previous studies, we found that males with higher social mating success (harem size) also tended to have higher within-pair paternity and that the number of extra-pair young a male sired increased significantly with his social mating success. Females that paired with mated males were not more likely to produce extra-pair young. In contrast, extra-pair paternity was significantly lower in the nests of females whose nesting activity overlapped that of another female on the same territory. This pattern of mating was robust to differences in breeding density. Indeed, breeding density had no effect on either extra-pair mating or on the association between polygyny and paternity. Finally, nest survival increased with harem size. This result, combined with the positive association between polygyny and paternity, contributed to significantly higher realized reproductive success by polygynous male dickcissels.

Keywords

Mating patterns Polygyny Extra-pair paternity Trade offs Female choice Density 

Notes

Acknowledgments

We thank the University of California at Berkeley’s Museum of Vertebrate Zoology for use of laboratory facilities for paternity analysis and Wayne Li, Lauren Scopel, and Dr. Sheila Byrne for help in the field. We appreciate the helpful comments on the MS from A. Pilastro, J. Lifjeld, and an anonymous reviewer. This study was supported by grants from the American Philosophical Society’s Lewis and Clark Fund for Field Research and The Gertrude Ribble Fund from the U.K. Department of Biology. B. Sousa was supported by a graduate fellowship from the Graduate School of the University of Kentucky. Konza Prairie Biological Station is a preserve of The Nature Conservancy managed by the Division of Biology at Kansas State University.

Ethical standards

The authors declare that all experiments comply with current US laws.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Alatalo RV, Lundberg A (1984) Polyterritorial polygyny in the Pied Flycatcher Ficedula hypoleuca—evidence for the deception hypothesis. Ann Zool Fenn 21:217–228Google Scholar
  2. Arak A (1984) Sneaky breeders. In: Barnard CJ (ed) Producers and scroungers. Croom Helm, Beckenham, pp 154–194CrossRefGoogle Scholar
  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 Lond B 269:1263–1269CrossRefGoogle Scholar
  4. Arnold SJ, Wade MJ (1984) On the measurement of natural and sexual selection: theory. Evolution 38:709–719CrossRefGoogle Scholar
  5. Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368PubMedCrossRefGoogle Scholar
  6. Berkeley LI, McCarty JP, Wolfenbarger LL (2007) Postfledging survival and movement in dickcissels (Spiza americana): implications for habitat management and conservation. Auk 124:396–409CrossRefGoogle Scholar
  7. Beyer HL (2010) Geospatial modelling environment. In, 0.3.3 Beta edn. Spatial Ecology LLCGoogle Scholar
  8. Birkhead TR (1978) Behavioral adaptations to high-density nesting in common Guillemot Uria-aalge. Anim Behav 26:321–324CrossRefGoogle Scholar
  9. Birkhead TR (1979) Mate guarding in the magpie Pica pica. Anim Behav 27:866–874CrossRefGoogle Scholar
  10. Bollinger EK, Gavin TA (1991) Patterns of extra-pair fertilizations in bobolinks. Behav Ecol Sociobiol 29:1–7CrossRefGoogle Scholar
  11. Borgia G (1979) Sexual selection and the evolution of matings systems. In: Blum MS, Blum NA (eds) Sexual selection and reproductive competition in insects. Academic, New York, pp 19–80Google Scholar
  12. Catchpole C, Slater PJB (2008) Bird song: biological themes and variations. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  13. Chomczynski P, Sacchi N (2006) The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on. Nat Protoc 1:581–585PubMedCrossRefGoogle Scholar
  14. Dawson, R.J.G., Gibbs, H.L., Hobson, K.A., and Yezerinac, S.M. (1997) Isolation of microsatellite DNA markers from a passerine bird, Dendroica petechia (the yellow warbler), and their use in population studies. Heredity 79:506-514Google Scholar
  15. Dechant JA, Sondreal ML, Johnson DH, Igl LD, Goldade CM, Zimmerman AL, Euliss BR (2003) Effects of management practices on grassland birds: dickcissel. In: Center NPWR (ed). Northern Prairie Wildlife Research Center, Jamestown pp 1–32Google Scholar
  16. Double MC, Dawson D, Burke T, Cockburn A (1997) Finding the fathers in the least faithful bird: a microsatellite-based genotyping system for the superb fairy-wren Malurus cyaneus. Mol Ecol 6:691–693CrossRefGoogle Scholar
  17. Dunn PO, Robertson RJ (1993) Extra-pair paternity in polygynous tree swallows. Anim Behav 45:231–239CrossRefGoogle Scholar
  18. Finck EJ (1983) Male behavior, territory quality and female choice in the dickcissel (Spiza americana). Kansas State University, DissertationGoogle Scholar
  19. Finck EJ (1984) Male dickcissel behavior in primary and secondary habitats. Wilson Bull 96:672–680Google Scholar
  20. Fiumera AC, Porter BA, Grossman GD, Avise JC (2002) Intensive genetic assessment of the mating system and reproductive success in a semi-closed population of the mottled sculpin, Cottus bairdi. Mol Ecol 11:2367–2377PubMedCrossRefGoogle Scholar
  21. Forstmeier W (2003) Extra-pair paternity in the dusky warbler, Phylloscopus fuscatus: a test of the ‘Constrained Female Hypothesis. Behaviour 140:1117–1134CrossRefGoogle Scholar
  22. Freeland JR, Hannon SJ, Dobush G, Boag PT (1995) Extra-pair paternity in willow ptarmigan broods: measuring costs of polygyny to males. Behav Ecol Sociobiol 36:349–355CrossRefGoogle Scholar
  23. Freeman-Gallant CR (1997) Extra-pair paternity in monogamous and polygynous Savanna sparrows. Passerculus sandwichensis Anim Behav 53:397–404CrossRefGoogle Scholar
  24. Freeman-Gallant CR, Wheelwright NT, Meiklejohn KE, States SL, Sollecito SV, Webster M (2005) Little effect of extrapair paternity on the opportunity for sexual selection in savannah sparrows (Passerculus sandwichensis). Evolution 59:422–430PubMedGoogle Scholar
  25. Fretwell SD (1986) Distribution and abundance of the dickcissel. Curr Ornith 4:211–242Google Scholar
  26. Frey CM, Jensen WE, With KA (2008) Topographic patterns of nest placement and habitat quality for grassland birds in tallgrass prairie. Am Midl Nat 160:220–234CrossRefGoogle Scholar
  27. Gibbs M, Dawson DA, McCamley C, Wardle AF, Armour JAL, Burke T (1997) Chicken microsatellite markers isolated from libraries enriched for simple tandem repeats. Anim Genet 28:401–417PubMedGoogle Scholar
  28. Gibbs HL, Tabak LM, Hobson K (1999) Characterization of microsatellite DNA loci for a neotropical migrant songbird, the Swainson's thrush (Catharus ustulatus). Mol Ecol 8:1551–1552CrossRefGoogle Scholar
  29. Gowaty PA (1996) Battles of the sexes and origins of monogamy. In: Black JM (ed) Partnerships in birds: the study of monogamy. Oxford University Press, New York, pp 21–52Google Scholar
  30. Gray EM (1998) Intraspecific variation in extra-pair behavior of red-winged blackbirds (Agelaius phoeniceus). Ornithol Monogr 49:61–80CrossRefGoogle Scholar
  31. 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
  32. Gross AO (1921) The dickcissel (Spiza americana) of the Illinois prairies. Auk 38:163–184CrossRefGoogle Scholar
  33. Hansson B, Bensch S, Hasselquist D (2000) Patterns of nest predation contribute to polygyny in the Great Reed Warbler. Ecology 81:319–328CrossRefGoogle Scholar
  34. Harmeson JP (1974) Breeding ecology of the dickcissel. Auk 91:348–359Google Scholar
  35. Hasselquist D (1998) Polygyny in great reed warblers: a long-term study of factors contributing to male fitness. Ecology 79:2376–2390CrossRefGoogle Scholar
  36. Hasselquist D, Bensch S (1991) Trade-off between mate guarding and mate attraction in the polygynous great reed warbler. Behav Ecol Sociobiol 28:187–193CrossRefGoogle Scholar
  37. Hasselquist D, Sherman PW (2001) Social mating systems and extrapair fertilizations in passerine birds. Behav Ecol 12:457–466CrossRefGoogle Scholar
  38. Heckel G, Von Helversen O (2003) Genetic mating system and the significance of harem associations in the bat Saccopteryx bilineata. Mol Ecol 12:219–227PubMedCrossRefGoogle Scholar
  39. Hill GE (2006) Female mate choice for ornamental coloration. In: Hill GE, McGraw KJ (eds) Bird coloration: function and evolution. Harvard University Press, Cambridge, pp 137–200Google Scholar
  40. Hughes JP, Robel RJ, Kemp KE, Zimmerman JL (1999) Effects of habitat on dickcissel abundance and nest success in conservation reserve program fields in Kansas. J Wildlife Manage 63:523–529CrossRefGoogle Scholar
  41. Hurvich CM, Tsai C-L (1989) Regression and time series model selection in small samples. Biometrika 76:297–307CrossRefGoogle Scholar
  42. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev Camb Philos Soc 75:21–64PubMedCrossRefGoogle Scholar
  43. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program cervus accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106PubMedCrossRefGoogle Scholar
  44. Kempenaers B, Verheyen GR, Dhondt AA (1995) Mate guarding and copulation behavior in monogamous and polygynous blue tits—do males follow a best-of-a-bad-job strategy. Behav Ecol Sociobiol 36:33–42CrossRefGoogle Scholar
  45. Knapp AK, Briggs JM, Hartnett DC, Collins SL (1998) Grassland dynamics: long-term ecological research in tallgrass prairie. Oxford University Press, New YorkGoogle Scholar
  46. Krackow S, Tkadlec E (2001) Analysis of brood sex ratios: implications of offspring clustering. Behav Ecol Sociobiol 50:293–301CrossRefGoogle Scholar
  47. Laird PW, Zijderveld A, Linders K, Rudnicki MA, Jaenisch R, Berns A (1991) Simplified mammalian DNA isolation procedure. Nucleic Acids Res 19:4293–4293PubMedCrossRefGoogle Scholar
  48. Lambert D (1992) Zero-inflated Poisson regression, with an application to defects in manufacturing. Technometrics 34:1–14CrossRefGoogle Scholar
  49. Lenington S (1980) Female choice and polygyny in redwinged blackbirds. Anim Behav 28:347–361CrossRefGoogle Scholar
  50. Lifjeld JT, Dunn PO, Westneat DF (1994) Sexual selection by sperm competition in birds: male–male competition or female choice? J Avian Biol 25:244–250CrossRefGoogle Scholar
  51. Ligon JD (1999) The evolution of avian breeding systems. Oxford University Press, New YorkGoogle Scholar
  52. Mayer C, Schiegg K, Pasinelli G (2008) Isolation, characterization and multiplex genotyping of 11 autosomal and four sex-linked microsatellite loci in the reed bunting, Emberiza schoeniclus (Emberizidae, Aves). Mol Ecol Resour 8:332–334PubMedCrossRefGoogle Scholar
  53. Mohr CO (1947) Table of equivalent populations of north american small mammals. Am Midl Nat 37:223–249CrossRefGoogle Scholar
  54. Moller AP, Birkhead TR (1993) Cuckoldry and sociality: a comparative study of birds. Am Nat 142:118–140PubMedCrossRefGoogle Scholar
  55. Moon JC, McCoy ED, Mushinsky HR, Karl SA (2006) Multiple paternity and breeding system in the gopher tortoise, Gopherus polyphemus. J Hered 97:150–157PubMedCrossRefGoogle Scholar
  56. Mulder RA, Dunn PO, Cockburn A, Lazenby-Cohen KA, Howell MJ (1994) Helpers liberate female fairy-wrens from constraints on extra-pair mate choice. Proc R Soc Lond B 255:223–229CrossRefGoogle Scholar
  57. Nol E, Smith JNM (1987) Effects of age and breeding experience on seasonal reproductive success in the song sparrow. J Anim Ecol 56:301–313CrossRefGoogle Scholar
  58. Odum EP, Kuenzler EJ (1955) Measurement of territory and home range size in birds. Auk 72:128–137CrossRefGoogle Scholar
  59. Orians GH (1969) On evolution of mating systems in birds and mammals. Am Nat 103:589–603CrossRefGoogle Scholar
  60. 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
  61. Payne RB (1979) Sexual selection and intersexual differences in variance of breeding success. Am Nat 114:447–452CrossRefGoogle Scholar
  62. Pilastro A, Griggio M, Biddau L, Mingozzi T (2002) Extrapair paternity as a cost of polygyny in the rock sparrow: behavioural and genetic evidence of the “trade-off” hypothesis. Anim Behav 63:967–974CrossRefGoogle Scholar
  63. Poesel A, Kunc HP, Foerster K, Johnsen A, Kempenaers B (2006) Early birds are sexy: male age, dawn song and extrapair paternity in blue tits, Cyanistes (formerly Parus) caeruleus. Anim Behav 72:531–538CrossRefGoogle Scholar
  64. Polakova R, Vyskocilova M, Martin JF, Mays HL, Hill GE, Bryja J, Albrecht T (2007) A multiplex set of microsatellite markers for the scarlet rosefinch (Carpodacus erythrinus). Mol Ecol Notes 7:1375–1378CrossRefGoogle Scholar
  65. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnol 18:233–234CrossRefGoogle Scholar
  66. Searcy WA, Yasukawa K (1989) Alternative models of territorial polygyny in birds. Am Nat 134:323–343CrossRefGoogle Scholar
  67. Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90CrossRefGoogle Scholar
  68. Smith HG (1995) Experimental demonstration of a trade-off between mate attraction and paternal care. Proc R Soc Lond B 260:45–51CrossRefGoogle Scholar
  69. Sousa BF, Stewart SLM (2011) Design and effectiveness of a novel trap for capturing nesting songbirds. J Field Ornithol 82:425–429CrossRefGoogle Scholar
  70. Stenzler LM, Fraser R, Lovette IJ (2004) Isolation and characterization of 12 microsatellite loci from golden-winged warblers (Vermivora chrysoptera) with broad cross-taxon utility in emberizine songbirds. Mol Ecol Notes 4:602–604CrossRefGoogle Scholar
  71. Stewart SLM, Westneat DF, Ritchison G (2010) Extra-pair paternity in eastern bluebirds: effects of manipulated density and natural patterns of breeding synchrony. Behav Ecol Sociobiol 64:463–473CrossRefGoogle Scholar
  72. Stutchbury BJ, Morton ES (1995) The effect of breeding synchrony on extra-pair mating systems in songbirds. Behaviour 132:675–690CrossRefGoogle Scholar
  73. Temple SA (2002) Dickcissel (Spiza americana). In: Poole A, Gill F (eds) The birds of North America, vol 703, The Birds of North America. Inc, Philadelphia, pp 1–23Google Scholar
  74. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179Google Scholar
  75. Trnka A, Prokop P (2010) Does social mating system influence nest defence behaviour in great reed warbler (Acrocephalus arundinaceus) males? Ethology 116:1075–1083CrossRefGoogle Scholar
  76. Vaclav R, Hoi H, Blomqvist D (2003) Food supplementation affects extrapair paternity in house sparrows (Passer domesticus). Behav Ecol 14:730–735CrossRefGoogle Scholar
  77. Vedder O, Komdeur J, van der Velde M, Schut E, Magrath M (2011) Polygyny and extra-pair paternity enhance the opportunity for sexual selection in blue tits. Behav Ecol Sociobiol 65:741–752PubMedCrossRefGoogle Scholar
  78. Verner J, Willson MF (1966) Influence of habitats on mating systems of north american passerine birds. Ecology 47:143–147CrossRefGoogle Scholar
  79. Weatherhead PJ (1999) Sequential mating patterns suggest extra-pair mating is not part of a mixed reproductive strategy by female red-winged blackbirds. Proc R Soc Lond B 266:1027–1031CrossRefGoogle Scholar
  80. Weatherhead, PJ, Boag, PT (1997) Genetic estimates of annual and lifetime reproductive success in male red-winged blackbirds. Ecology 78:884-896Google Scholar
  81. Weatherhead PJ, Boag PT (1995) Pair and extra-pair mating success relative to male quality in red-winged blackbirds. Behav Ecol Sociobiol 37:81–91CrossRefGoogle Scholar
  82. Weatherhead PJ, Robertson RJ (1977) Harem size, territory quality, and reproductive success in the redwinged blackbird (Agelaius phoeniceus). Can J Zool 55:1261–1267CrossRefGoogle Scholar
  83. Weatherhead PJ, Robertson RJ (1979) Offspring quality and the polygyny threshold—sexy son hypothesis. Am Nat 113:201–208CrossRefGoogle Scholar
  84. Werren JH, Gross MR, Shine R (1980) Paternity and the evolution of male parental care. J Theor Biol 82:619–631PubMedCrossRefGoogle Scholar
  85. Westneat DF (1993) Polygyny and extrapair fertilizations in eastern red-winged blackbirds (Agelaius phoeniceus). Behav Ecol 4:49–60CrossRefGoogle Scholar
  86. Westneat DF (1994) To guard mates or go forage: conflicting demands affect the paternity of male red-winged blackbirds. Am Nat 144:343–354CrossRefGoogle Scholar
  87. Westneat DF, Sherman PW (1993) Parentage and the evolution of parental behavior. Behav Ecol 4:66–77CrossRefGoogle Scholar
  88. Westneat DF, Sherman PW, Morton ML (1990) The ecology and evolution of extra-pair copulations in birds. Curr Ornithol 7:331–369Google Scholar
  89. White GC, Burnham KP (1999) Program MARK: Survival estimation from populations of marked animals. Bird Study 46:120–138CrossRefGoogle Scholar
  90. Woodcock EA, Rathburn MK, Ratcliffe LM (2005) Achromatic plumage reflectance, social dominance and female mate preference in black-capped chickadees (Poecile atricapillus). Ethology 111:891–900CrossRefGoogle Scholar
  91. Wright J (1998) Paternity and paternal care. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic, San Diego, pp 117–145CrossRefGoogle Scholar
  92. Yasukawa K, Whittenberger LK, Nielsen TA (1992) Anti-predator vigilance in the red-winged blackbird, Agelaius phoeniceus: do males act as sentinels? Anim Behav 43:961–969CrossRefGoogle Scholar
  93. Zimmerman JL (1966) Polygyny in the dickcissel. Auk 83:534–546CrossRefGoogle Scholar
  94. Zimmerman JL (1971) Territory and its density dependent effect in Spiza americana. Auk 88:591–612Google Scholar
  95. Zimmerman JL (1982) Nesting success of dickcissels (Spiza americana) in preferred and less preferred habitats. Auk 99:292–298Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Department of Biology, Center for Ecology, Evolution, and BehaviorUniversity of KentuckyLexingtonUSA

Personalised recommendations