Behavioral Ecology and Sociobiology

, Volume 27, Issue 1, pp 67–76 | Cite as

Genetic parentage in the indigo bunting: a study using DNA fingerprinting

  • David F. Westneat
Article

Summary

Parentage of nestlings in a North Carolina population of indigo buntings (Passerina cyanea) was analyzed using DNA fingerprinting. Three minisatellite DNA probes (wild type M13, Jeffreys' 33.15 and 33.6) were used to analyze nuclear DNA isolated from muscle biopsies of 63 nestlings, their parents, and other local adults. Each probe detected approximately 15 scorable fragments per individual, with 18%–39% overlap between probes. The proportion of bands shared (using all fragments over all three probes) between presumably unrelated adults averaged 0.23. Of the 63 offspring analyzed, 35 had at least one fragment not present in either putative parent. The distribution of offspring with novel fragments was distinctly bimodal. The lower mode (offspring with 0, 1, or 2 novel fragments, N=41) fit a Poisson distribution, a pattern expected if mutation (estimated rate per fragment= 0.01) were the source of the novel fragments. The remaining 22 offspring had more novel fragments than could be explained by mutation alone (minimum of four independent fragments across all three probes, \(\bar X\)=8.2). A low band-sharing proportion with the resident male (\(\bar X\)=0.24) and high band-sharing with the resident female (\(\bar X\)=0.60) implicated extra-pair fertilizations as the source of all 22. Thus in this sample, 35% of all nestlings came from extra-pair fertilizations and none from intra-specific brood parasitism. Of 25 broods sampled, 12 (48%) had at least one excluded offspring. In 3 broods all of the offspring excluded the resident male. Band-sharing proportions between excluded nestlings within a brood could not distinguish between single and multiple extra-pair paternity. Although young males tended to be excluded less often than older males, wing length and weight were not associated with the frequency of exclusion. Weight and wing length of females also were not associated with involvement in EPCs. Six of the 22 excluded offspring (in 3 broods) shared a large proportion of bands and had fewer than four novel fragments when compared to the fingerprints of a neighboring territorial male, implicating those males as actual fathers. The parentage of the remaining 16 offspring (in 9 broods) could not be clearly assigned because (1) one or more neighbors were not sampled or (2) difficulties in scoring across gels prevented confident alignment of fingerprint bands, and insufficient DNA was obtained from muscle samples to allow reanalysis of potential actual fathers on the same gel as excluded nestlings.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alatalo RV, Gustafsson L, Lundberg A (1984) High frequency of cuckoldry in pied and collared flycatchers. Oikos 42:41–47Google Scholar
  2. Birkhead TR, Pellatt J, Hunter FM (1988) Extra-pair copulation and sperm competition in the zebra finch. Nature 334:60–62Google Scholar
  3. Brown CR, Bomberger Brown M (1988) Genetic evidence of multiple parentage in broods of cliff swallows. Behav Ecol Sociobiol 23:379–387Google Scholar
  4. Burke T, Bruford MW (1987) DNA fingerprinting in birds. Nature 327:149–152Google Scholar
  5. Burke T, Davies NB, Bruford MW, Hatchwell BJ (1989) Parental care and mating behaviour of polyandrous dunnocks Prunella modularis related to paternity by DNA fingerprinting. Nature 338:249–251Google Scholar
  6. Burns JT, Cheng KM, McKinney F (1980) Forced copulation in captive mallards. I. Fertilization of eggs. Auk 97:875–879Google Scholar
  7. Carey M, Nolan V (1979) Population dynamics of indigo buntings and the evolution of avian polygyny. Evolution 33:1180–1192Google Scholar
  8. Chakraborty R, Meagher TR, Smouse PE (1988) Parentage analysis with genetic markers in natural populations. I. The expected proportion of offspring with unambiguous paternity. Genetics 118:527–536Google Scholar
  9. Cooke F, Mirsky PJ (1972) A genetic analysis of lesser snow goose families. Auk 89:863–871Google Scholar
  10. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  11. Evarts S, Williams CJ (1987) Multiple paternity in a wild population of mallards. Auk 104:597–602Google Scholar
  12. Gavin TA, Bollinger EK (1985) Multiple paternity in a territorial passerine: the bobolink. Auk 102: 550–555Google Scholar
  13. Gowaty PA (1985) Multiple parentage and apparent monogamy in birds. Ornithol Monogr 37:11–21Google Scholar
  14. Gowaty PA, Karlin AA (1984) Multiple maternity and paternity in single broods of apparently monogamous eastern bluebirds (Sialia sialis). Behav Ecol Sociobiol 15:91–95Google Scholar
  15. Gyllensten UB, Jakobsson S, Temrin H, Wilson AC (1989) Nucleotide sequence and genomic organization of bird minisatellites. Nucleic Acids Res 17:2203–2214Google Scholar
  16. Gyllensten UB, Jakobsson S, Temrin H (1990) No evidence for illegitimate young in monogamous and polygynous warblers. Nature 343:168–170Google Scholar
  17. Hoffenberg AS, Power HW, Romagnano LC, Lombardo MP, McGuire TR (1988) The frequency of cuckoldry in the European starling (Sturnus vulgaris). Wilson Bull 100:60–69Google Scholar
  18. Jeffreys AJ, Wilson V, Thein SL (1985) Hypervariable ‘minisatel-lite’ regions in human DNA. Nature 314:67–73Google Scholar
  19. Jeffreys AJ, Wilson V, Kelly R, Taylor BA, Bulfield G (1987) Mouse DNA ‘fingerprints’: analysis of chromosome location and germline stability of hypervariable loci in recombinant inbred strains. Nucleic Acids Res 15:2823–2836Google Scholar
  20. Lank DB, Mineau P, Rockwell RF, Cooke F (1989) Intraspecific nest parasitism and extra-pair copulation in lesser snow geese. Anim Behav 37:74–89Google Scholar
  21. Lynch M (1988) Estimation of relatedness by DNA fingerprinting. Mol Biol Evol 5:584–599Google Scholar
  22. Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory. Cold Spring Harbor, NYGoogle Scholar
  23. Møller AP (1987) Behavioural aspects of sperm competition in swallows (Hirundo rustica). Behaviour 100:92–104Google Scholar
  24. Mumme RL, Koenig WD, Zink RM, Marten JA (1985) Genetic variation and parentage in a California population of acorn woodpeckers. Auk 102:305–312Google Scholar
  25. Norris KJ, Blakey JK (1989) Evidence for cuckoldry in the Great Tit Parus major. Ibis 131:436–441Google Scholar
  26. Payne RB (1982) Ecological consequences of song matching: breeding success and intraspecific mimicry in indigo buntings. Ecology 63:401–411Google Scholar
  27. Payne RB, Payne LL (1989) Heritability estimates and behavior observations: extra-pair matings in indigo buntings. Anim Behav 38:457–567Google Scholar
  28. Payne RB, Payne LL, Doehlert SM (1987) Song, mate choice and the question of kin recognition in a migratory songbird. Anim Behav 35:35–47Google Scholar
  29. Quinn TW, White BN (1987) Identification of restriction-fragment-length polymorphisms in genomic DNA of the lesser snow goose (Anser caerulescens caerulescens). Mol Biol Evol 4:126–143Google Scholar
  30. Reeve HK, Westneat DF, Noon WA, Sherman PW, Aquadro CF (1990) DNA ‘fingerprinting’ reveals high levels of inbreeding in colonies of the eusocial naked mole-rat. Proc Natl Acad Sci 87:2496–2500Google Scholar
  31. Selander RK, Smith MH, Yang SY, Johnson WE, Gentry JE (1971) Biochemical polymorphism and systematics in the genus Peromyscus. I. Variation in the old field mouse (Peromyscus polionotus). Univ Texas Publ 7103:49–90Google Scholar
  32. Sherman PW, Morton ML (1988) Extra-pair fertilizations in mountain white-crowned sparrows. Behav Ecol Sociobiol 22:413–420Google 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 136–179Google Scholar
  34. Vassart G, Georges M, Monsieur R, Brocas H, Lequarre AS, Christophe D (1987) A sequence in M13 phage detects hypervariable minisatellites in human and animal DNA. Science 235:683–684Google Scholar
  35. Westneat DF (1987a) Extra-pair fertilizations in a predominantly monogamous bird: genetic evidence. Anim Behav 35:877–886Google Scholar
  36. Westneat DF (1987b) Extra-pair copulations in a predominantly monogamous bird: observations of behaviour. Anim Behav 35:865–876Google Scholar
  37. Westneat DF (1988a) Parental care and extrapair copulations in the indigo bunting. Auk 105:149–160Google Scholar
  38. Westneat DF (1988b) The relationships among polygyny, male parental care, and female breeding success in the indigo bunting. Auk 105:372–374Google Scholar
  39. Westneat DF, Payne RB, Doehlert SM (1986) Effects of muscle biopsy on survival and breeding success in indigo buntings. Condor 88:220–227Google Scholar
  40. Westneat DF, Frederick PC, Wiley RH (1987) The use of genetic markers to estimate the frequency of successful alternative reproductive tactics. Behav Ecol Sociobiol 21:35–45Google Scholar
  41. Westneat DF, Noon WA, Reeve HK, Aquadro CF (1988) Improved hybridization conditions for DNA ‘fingerprints’ probed with M13. Nucleic Acids Res 16:4161Google Scholar
  42. Wetton JH, Carter RE, Parkin DT, Walters D (1987) Demographic study of a wild house sparrow population by DNA fingerprinting. Nature 327:147–149Google Scholar
  43. Wong Z, Wilson V, Jeffreys AJ, Them SL (1986) Cloning a selected fragment from a human DNA ‘fingerprint’: isolation of an extremely polymorphic minisatellite. Nucleic Acids Res 14:4605–4616Google Scholar
  44. Wrege PH, Emlen ST (1987) Biochemical determination of parental uncertainty in white-fronted bee-eaters. Behav Ecol Sociobiol 20:153–160Google Scholar

Copyright information

© Springer-Verlag 1990

Authors and Affiliations

  • David F. Westneat
    • 1
  1. 1.Section of Genetics and DevelopmentCornell UniversityIthacaNYUSA

Personalised recommendations