Conservation Genetics

, Volume 5, Issue 3, pp 339–348 | Cite as

Marker-Based Relatedness Predicts Egg-Hatching Failure in Great Reed Warblers

  • Bengt Hansson


I examine the relationship between reproductive success and marker-based relatedness (MBR; inferred from variation at 21 microsatellite loci) of pair-mates in a semi-isolated population of great reed warblers (Acrocephalus arundinaceus) over a 12 year period. There was a negative relationship between egg-hatching success and MBR, but no association between MBR and three other components of fitness (clutch size, proportion of fledglings and recruits). The relationship between hatchability and MBR was non-linear, with high hatching rates at low and intermediate levels of MBR and a sudden decline in hatching success among the small number of pairs with high MBR (<4% of the sample). It is likely that the decrease in fitness at high MBR was due to effects of homozygosity at genome-wide distributed loci, as opposed to effects of fitness loci in the local chromosomal vicinity of particular markers. This conclusion relies on the fact that similar results were found in another study of the same population that was based on DNA-fingerprinting band-sharing, and that there was a strong correlation between MBR and pedigree-based relatedness. The negative relationship between MBR and hatchability was especially pronounced in the first study years and levelled off in later years. This time-dependent effect of MBR on hatchability was not caused by a simultaneous temporal decrease in MBR, and may instead reflect the importance of other processes such as genotype × environment interactions or purging of deleterious recessive alleles.

inbreeding inbreeding depression relatedness microsatellite great reed warbler 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Bensch S (1996) Female mating status and reproductive success in the great reed warbler: Is there a potential cost of polygyny that requires compensation? J. Anim. Ecol., 65, 283–296.Google Scholar
  2. Bensch S, Hasselquist D (1999) Phylogeographic population structure of great reed warblers: An analysis of mtDNA control region sequences. Biol. J. Linn. Soc., 66, 171–185.Google Scholar
  3. Bensch S, Hasselquist D, von Schantz T (1994) Genetic similarity between parents predicts hatching failure: Noninces tuous inbreeding in the great reed warbler. Evolution, 48, 317–326.Google Scholar
  4. Bensch S, Hasselquist D, Nielsen B, Hansson B (1998) Higher fitness for philopatric than for immigrant males in a semi-isolated population of great reed warblers. Evolution, 52, 877–883.Google Scholar
  5. Bensch S, Hansson B, Hasselquist D, Nielsen B (2000) Partial albinism in a semi-isolated population of great reed warblers. Hereditas, 133, 167–170.PubMedGoogle Scholar
  6. Bijlsma R, Bundgaard J, Boerema AC (2000) Does inbreeding affect the extinction risk of small populations? Predictions from Drosophila. J. Evol. Biol., 13, 502–514.Google Scholar
  7. Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst., 18, 237–268.Google Scholar
  8. Coulson TN, Pemberton JM, Albon SD, Beaumont M, Marshall TC, Slate J, Guinness FE, Clutton-Brock TH (1998) Microsatellites reveal heterosis in red deer. Proc. R. Soc. Lond. B, 265, 489–495.Google Scholar
  9. Coulson T, Albon S, Slate J, Pemberton J (1999) Microsatellite loci reveal sex-dependent responses to inbreeding and out-breeding in red deer calves. Evolution, 53, 1951–1960.Google Scholar
  10. Cramp S (1992) Handbook of the Birds of Europe, the MiddleEast and North Africa. Vol VI. Oxford University Press, New York.Google Scholar
  11. Crawley MJ (1993) GLIM for Ecologists. Blackwell Scientific Publications, Oxford.Google Scholar
  12. Crnokrak P, Roff DA (1999) Inbreeding depression in the wild. Heredity, 83, 260–270.PubMedGoogle Scholar
  13. Dallas JF (1992) Estimation of microsatellite mutation rates in recombinant inbred strains of mouse. Mammalian Genome, 3, 452–456.PubMedGoogle Scholar
  14. David P (1998) Heterozygosity-fitness correlations: New perspective on old problems. Heredity, 80, 531–537.PubMedGoogle Scholar
  15. Di Rienzo A, Donnelly P, Toomajian C, Sisk B, Hill A, Petzl-Erler ML, Haines GK, Barch DH (1998) Heterogeneity of microsatellite mutations within and between loci, and implications for the human demographic histories. Genetics, 148, 1269–1284.PubMedGoogle Scholar
  16. Dudash MR (1990) Relative fitness of selfed and outcrossed progeny in a self-compatible, protandrous species, Sabatia angularis L. (Gentianaceae): A comparison in three environments. Evolution, 44, 1129–1139.Google Scholar
  17. Hansson B (2003) Dispersal, Inbreeding and Fitness in Natural Populations. PhD thesis, Department of Ecology, Lund University, Sweden.Google Scholar
  18. Hansson B, Westerberg L (2002) On the correlation between heterozygosity and fitness in natural populations. Mol. Ecol., 11, 2467–2474.PubMedGoogle Scholar
  19. Hansson B, Bensch S, Hasselquist D (2000a) The quality and the timing hypotheses evaluated using data on great reed warblers. Oikos, 90, 575–581.CrossRefGoogle Scholar
  20. Hansson B, Bensch S, Hasselquist D, Lillandt B-G, Wennerberg L, von Schantz T (2000b) Increase of genetic variation over time in a recently founded population of great reed warblers (Acrocephalus arundinaceus) revealed by microsatellites and DNA fingerprinting. Mol. Ecol., 9, 1529–1538.PubMedGoogle Scholar
  21. Hansson B, Bensch S, Hasselquist D, Åkesson M (2001) Microsatellite diversity predicts recruitment of sibling great reed warblers. Proc. R. Soc. Lond. B, 268, 1287–1291.Google Scholar
  22. Hansson B, Bensch S, Hasselquist D, Nielsen B (2002) Restricted dispersal in a long-distance migrant bird with patchy distribution, the great reed warbler. Oecologia, 130, 536–542.Google Scholar
  23. Hansson B, Bensch S, Hasselquist D (2003) A new approach to study dispersal: Immigration of novel alleles reveals female-biased dispersal in great reed warblers. Mol. Ecol., 12, 631–637.PubMedGoogle Scholar
  24. Hasselquist D (1998) Polygyny in the great reed warbler: A long-term study of factors contributing to male fitness. Ecology, 79, 2376–2390.Google Scholar
  25. Hasselquist D, Bensch S, von Schantz T (1995) Low frequency of extra-pair paternity in the polygynous great reed warbler. Behav. Ecol., 6, 27–38.Google Scholar
  26. Hasselquist D, Bensch S, von Schantz T (1996) Correlation between male song repertoire, extra-pair paternity and off-spring survival in the great reed warbler. Nature, 381, 229–232.CrossRefGoogle Scholar
  27. Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annu. Rev. Ecol. Syst., 31, 139–162.Google Scholar
  28. Hughes CR, Queller DC (1993) Detection of highly polymorphic microsatellite loci in a species with little allozyme polymorphism. Mol. Ecol., 2, 131–137.PubMedGoogle Scholar
  29. Kalinowski ST, Hedrick PW, Miller PS (2000) Inbreeding depression in the Speke’s gazelle captive breeding program. Conserv. Biol., 14, 1375–1384.Google Scholar
  30. Keller LF (1998) Inbreeding and its fitness effects in an insular population of song sparrows (Melospiza melodia). Evolution, 52, 240–250.Google Scholar
  31. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol. Evol., 17, 230–241.Google Scholar
  32. Kempenaers B, Adriaensen F, Dhondt AA (1998) Inbreeding and divorce in blue and great tits. Anim. Behav., 56, 737–740.PubMedGoogle Scholar
  33. Kruuk LEB, Sheldon BC, Merilä J (2002) Severe inbreeding depression in collared flycatchers (Ficedula albicollis). Proc. R. Soc. Lond. B, 269, 1581–1589.Google Scholar
  34. LeBas NR (2002) Mate choice, genetic incompatibility, and outbreeding depression in the ornate dragon lizard, Ctenophorus ornatus. Evolution, 56, 371–377.PubMedGoogle Scholar
  35. Lynch M, Walsh B (1998) Genetics and Analysis of Quantitative Traits. Sinauer Associates, Inc., Sunderland.Google Scholar
  36. Marr AB, Keller LF, Arcese P (2002) Heterosis and out-breeding depression in descendants of natural immigrants to an inbred population of song sparrows (Melospiza melodia). Evolution, 56, 131–142.PubMedGoogle Scholar
  37. Marshall TC, Spalton JA (2000) Simultaneous inbreeding and outbreeding depression in reintroduced Arabian oryx. Anim. Conserv., 3, 241–248.Google Scholar
  38. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol. Ecol., 7, 639–655.PubMedGoogle Scholar
  39. Martinez JG, Soler JJ, Soler M, Møller AP, Burke T (1999) Comparative population structure and gene flow of a brood parasite, the great spotted cuckoo (Clamator glandarius), and its primary host, the magpie (Pica pica). Evolution, 53, 269–278.Google Scholar
  40. McDonald DB, Potts WK (1994) Cooperative display and relatedness among males in a lek-mating bird. Science, 266, 1030–1032.PubMedGoogle Scholar
  41. Mitton JB (1997) Selection in Natural Populations. Oxford University Press, Oxford.Google Scholar
  42. Nishiumi I, Yamagishi S, Maekawa H, Shimoda C (1996) Paternal expenditure is related to brood sex ratio in polygynous great reed warblers. Behav. Ecol. Sociobiol., 39, 211–217.Google Scholar
  43. Pemberton JM, Slate J, Bancroft DR, Barrett JA (1995) No-namplifying alleles at microsatellite loci-a caution for parentage and population studies. Mol. Ecol., 4, 249–252.PubMedGoogle Scholar
  44. Price MV, Waser NM (1979) Pollen dispersal and optimal outcrossing in Delphinium nelsoni. Nature, 277, 294–297.Google Scholar
  45. Primmer CR, Moller AP, Ellegren H (1996) A wide-range survey of cross-species microsatellite amplification in birds. Mol. Ecol., 5, 365–378.PubMedGoogle Scholar
  46. Queller DC, Goodnight K (1989) Estimating relatedness using genetic markers. Evolution, 43, 258–275.Google Scholar
  47. Ralls K, Ballou J (1986) Captive breeding programs for populations with a small number of founders. Trends Ecol. Evol., 1, 19–22.Google Scholar
  48. 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, 2155–2234.Google Scholar
  49. Ritland K (1996) Estimators for pairwise relatedness and individual inbreeding coefficients. Genet. Res., 67,175–185.CrossRefGoogle Scholar
  50. SAS Institute (1990) SAS Procedures Guide. Version 6, 3rd edn. SAS Institute, Cary, North Carolina, USA.Google Scholar
  51. Slate J, Pemberton J (2002) Comparing molecular measures for detecting inbreeding depression. J. Evol. Biol., 15, 20–31.Google Scholar
  52. Thelen GC, Allendorf FW (2001) Heterozygosity-fitness correlations in rainbow trout: Effects of allozyme loci or associative overdominance? Evolution, 55, 1180–1187.PubMedGoogle Scholar
  53. Tsitrone A, Rousset F, David P (2001) Heterosis, marker mutational processes and population inbreeding history. Genetics, 159, 1845–1859.PubMedGoogle Scholar
  54. van Noordwijk AJ, Scharloo W (1981) Inbreeding in an island population of the great tit. Evolution, 35, 674–688.Google Scholar
  55. Westemeier RL, Brawn JD, Simpson SA, Esker TL, Jansen RW, Walk JW, Kershner WL, Bouzat JL, Paige KN (1998) Tracking the long-term decline and recovery of an isolated population. Science, 282, 1695–1698.PubMedGoogle Scholar
  56. Wiener G, Lee GJ, Woolliams JA (1992) Effects of rapid inbreeding and of crossing of inbred lines on conception rate prolificacy and ewe survival in sheep. Anim. Prod., 55, 115–121.CrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • Bengt Hansson
    • 1
    • 2
  1. 1.Department of Animal EcologyLund University Ecology BuildingLundSweden
  2. 2.Institute of Cell, Animal and Population BiologyUniversity of EdinburghEdinburghUK; fax:

Personalised recommendations