Heterozygosity and survival in blue tits (Cyanistes caeruleus): Contrasting effects of presumably functional and neutral loci

Molecular Ecology

Volumn 20, Issue 19, 2011, Pages 4028-4041

  Olano Marin, Juanita ^a   Mueller, Jakob C ^a   Kempenaers, Bart ^a  

^a MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

Author keywords

expressed sequence tag; full sibling design; heterozygosity fitness correlation; inbreeding; microsatellites; negative heterozygosity fitness correlation

Indexed keywords

MICROSATELLITE DNA;

ANIMAL; ARTICLE; CHROMOSOME MAP; FEMALE; FINCH; GENETIC MARKER; GENETICS; GENOTYPE; HETEROZYGOTE; INBREEDING; LONGEVITY; MALE; PHYSIOLOGY; SONGBIRD;

ANIMALS; CHROMOSOME MAPPING; FEMALE; FINCHES; GENETIC MARKERS; GENOTYPE; HETEROZYGOTE; INBREEDING; LONGEVITY; MALE; MICROSATELLITE REPEATS; PASSERIFORMES;

CYANISTES CAERULEUS; TAENIOPYGIA GUTTATA;

EID: 80053291055     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2011.05177.x     Document Type: Article

References (68)

1. Aparicio JM, Ortego J, Cordero PJ, (2006) What should we weigh to estimate heterozygosity, alleles or loci? Molecular Ecology, 15, 4659-4665. (Pubitemid 44749577)
2. Balloux F, Amos W, Coulson T, (2004) Does heterozygosity estimate inbreeding in real populations? Molecular Ecology, 13, 3021-3031. (Pubitemid 39290228)
3. Bates D, Maechler M, (2010) lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-34.
4. Bell G, (2010) Fluctuating selection: the perpetual renewal of adaptation in variable environments. Philosophical Transactions of the Royal Society B-Biological Sciences, 365, 87-97.
5. Blomqvist D, Pauliny A, Larsson M, Flodin LA, (2010) Trapped in the extinction vortex? Strong genetic effects in a declining vertebrate population. BMC Evolutionary Biology, 10, 33.
6. Britten HB, (1996) Meta-analyses of the association between multilocus heterozygosity and fitness. Evolution, 50, 2158-2164. (Pubitemid 27114655)
7. Chapman JR, Nakagawa S, Coltman DW, Slate J, Sheldon BC, (2009) A quantitative review of heterozygosity-fitness correlations in animal populations. Molecular Ecology, 18, 2746-2765.
8. Charlesworth D, Willis JH, (2009) The genetics of inbreeding depression. Nature Reviews Genetics, 10, 783-796.
9. Charpentier M, Setchell JM, Prugnolle F, et al. (2006) Life history correlates of inbreeding depression in mandrills (Mandrillus sphinx). Molecular Ecology, 15, 21-28.
10. Coltman DW, Slate J, (2003) Microsatellite measures of inbreeding: a meta-analysis. Evolution, 57, 971-983. (Pubitemid 36726555)
11. Coltman DW, Pilkington JG, Smith JA, Pemberton JM, (1999) Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evolution, 53, 1259-1267. (Pubitemid 29416966)
12. Coulon A, (2010) GENHET: an easy-to-use R function to estimate individual heterozygosity. Molecular Ecology Resources, 10, 167-169.
13. Coulson TN, Pemberton JM, Albon SD, et al. (1998) Microsatellites reveal heterosis in red deer. Proceedings of the Royal Society of London Series B-Biological Sciences, 265, 489-495. (Pubitemid 28140303)
14. 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, 1951-1960. (Pubitemid 30044825)
15. Crnokrak P, Roff DA, (1999) Inbreeding depression in the wild. Heredity, 83, 260-270. (Pubitemid 29498795)
16. David P, (1998) Heterozygosity-fitness correlations: new perspectives on old problems. Heredity, 80, 531-537. (Pubitemid 28276295)
17. Dawson DA, Burke T, Hansson B, et al. (2006) A predicted microsatellite map of the passerine genome based on chicken-passerine sequence similarity. Molecular Ecology, 15, 1299-1320.
18. Delhey K, Johnsen A, Peters A, Andersson S, Kempenaers B, (2003) Paternity analysis reveals opposing selection pressures on crown coloration in the blue tit (Parus caeruleus). Proceedings of the Royal Society of London Series B-Biological Sciences, 270, 2057-2063. (Pubitemid 37211145)
19. DeWoody YD, DeWoody JA, (2005) On the estimation of genome-wide heterozygosity using molecular markers. Journal of Heredity, 96, 85-88.
20. Dhondt AA, Kempenaers B, Adriaensen F, (1992) Density-dependent clutch size caused by habitat heterogeneity. Journal of Animal Ecology, 61, 643-648. (Pubitemid 23397880)
21. 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. Molecular Ecology, 17, 783-795.
22. Foerster K, Delhey K, Johnsen A, Lifjeld JT, Kempenaers B, (2003) Females increase offspring heterozygosity and fitness through extra-pair matings. Nature, 425, 714-717. (Pubitemid 37314313)
23. FossÃy F, Johnsen A, Lifjeld JT, (2009) Cell-mediated immunity and multi-locus heterozygosity in bluethroat nestlings. Journal of Evolutionary Biology, 22, 1954-1960.
24. Fox CW, Scheibly KL, Wallin WG, Hitchcock LJ, Stillwell RC, Smith BP, (2006) The genetic architecture of life span and mortality rates: gender and species differences in inbreeding load of two seed-feeding beetles. Genetics, 174, 763-773. (Pubitemid 44656465)
25. Garcia-Navas V, Ortego J, Sanz JJ, (2009) Heterozygosity-based assortative mating in blue tits (Cyanistes caeruleus): implications for the evolution of mate choice. Proceedings of the Royal Society B-Biological Sciences, 276, 2931-2940.
26. Griffiths R, Double MC, Orr K, Dawson RJG, (1998) A DNA test to sex most birds. Molecular Ecology, 7, 1071-1075. (Pubitemid 28371645)
27. Hansson B, Westerberg L, (2002) On the correlation between heterozygosity and fitness in natural populations. Molecular Ecology, 11, 2467-2474. (Pubitemid 35436669)
28. Hansson B, Westerberg L, (2008) Heterozygosity-fitness correlations within inbreeding classes: local or genome-wide effects? Conservation Genetics, 9, 73-83.
29. Hansson B, Bensch S, Hasselquist D, Akesson M, (2001) Microsatellite diversity predicts recruitment of sibling great reed warblers. Proceedings of the Royal Society of London Series B-Biological Sciences, 268, 1287-1291. (Pubitemid 32622383)
30. Hansson B, Westerdahl H, Hasselquist D, Akesson M, Bensch S, (2004) Does linkage disequilibrium generate heterozygosity-fitness correlations in great reed warblers? Evolution, 58, 870-879. (Pubitemid 38583874)
31. International Chicken Genome Sequencing Consortium (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature, 432, 695-716.
32. Jarne P, Lagoda PJL, (1996) Microsatellites, from molecules to populations and back. Trends in Ecology & Evolution, 11, 424-429. (Pubitemid 126394588)
33. Jensen H, Bremset EM, Ringsby TH, S'ther BE, (2007) Multilocus heterozygosity and inbreeding depression in an insular house sparrow metapopulation. Molecular Ecology, 16, 4066-4078. (Pubitemid 47481044)
34. Keller LF, Waller DM, (2002) Inbreeding effects in wild populations. Trends in Ecology & Evolution, 17, 230-241. (Pubitemid 34270584)
35. Kempenaers B, Adriaensen F, vanNoordwijk AJ, Dhondt AA, (1996) Genetic similarity, inbreeding and hatching failure in blue tits: are unhatched eggs infertile? Proceedings of the Royal Society of London Series B-Biological Sciences, 263, 179-185.
36. Kimura M, (1983) Rare variant alleles in the light of the neutral theory. Molecular Biology and Evolution, 1, 84-93. (Pubitemid 15177342)
37. Krokene C, Lifjeld JT, (2000) Variation in the frequency of extra-pair paternity in birds: a comparison of an island and a mainland population of blue tits. Behaviour, 137, 1317-1330. (Pubitemid 33213720)
38. Kupper C, Kosztolanyi A, Augustin J, Dawson DA, Burke T, Szekely T, (2010) Heterozygosity-fitness correlations of conserved microsatellite markers in Kentish plovers Charadrius alexandrinus. Molecular Ecology, 19, 5172-5185.
39. Li YC, Korol AB, Fahima T, Nevo E, (2004) Microsatellites within genes: structure, function, and evolution. Molecular Biology and Evolution, 21, 991-1007. (Pubitemid 38658207)
40. Lieutenant-Gosselin M, Bernatchez L, (2006) Local heterozygosity-fitness correlations with global positive effects on fitness in three spine stickleback. Evolution, 60, 1658-1668. (Pubitemid 44808257)
41. Lynch M, (1991) The genetic interpretation of inbreeding depression and outbreeding depression. Evolution, 45, 622-629.
42. Markert JA, Grant PR, Grant BR, Keller LF, Coombs JL, Petren K, (2004) Neutral locus heterozygosity, inbreeding, and survival in Darwin's ground finches (Geospiza fortis and G. scandens). Heredity, 92, 306-315. (Pubitemid 38484994)
43. Marshall TC, Spalton JA, (2000) Simultaneous inbreeding and outbreeding depression in reintroduced Arabian oryx. Animal Conservation, 3, 241-248.
44. Mitton JB, Schuster WSF, Cothran EG, Defries JC, (1993) Correlation between the individual heterozygosity of parents and their offspring. Heredity, 71, 59-63.
45. Mueller JC, Hermisson J, Olano-Marin J, Hansson B, Kempenaers B, (2010) Linking genetic mechanisms of heterozygosity-fitness correlations to footprints of selection at single loci. Evolutionary Ecology, 25, 1-11.
46. Neff BD, (2004) Stabilizing selection on genomic divergence in a wild fish population. Proceedings of the National Academy of Sciences of the United States of America, 101, 2381-2385. (Pubitemid 38269320)
47. Olano-Marin J, Dawson DA, Girg A, et al. (2010) A genome-wide set of 106 microsatellite markers for the blue tit (Cyanistes caeruleus). Molecular Ecology Resources, 10, 516-532.
48. Olano-Marin J, Mueller JC, Kempenaers B, (2011) Correlations between heterozygosity and reproductive success in the blue tit (Cyanistes caeruleus): an analysis of inbreeding and single locus effects. Evolution, in press, DOI:.
49. Oliveira KM, Pinto LR, Marconi TG, et al. (2009) Characterization of new polymorphic functional markers for sugarcane. Genome, 52, 191-209.
50. Ortego J, Calabuig G, Cordero PJ, Aparicio JM, (2007) Egg production and individual genetic diversity in lesser kestrels. Molecular Ecology, 16, 2383-2392. (Pubitemid 46897163)
51. Pemberton J, (2004) Measuring inbreeding depression in the wild: the old ways are the best. Trends in Ecology & Evolution, 19, 613-615. (Pubitemid 39471289)
52. Pinheiro CJ, Bates MD, (2000) Mixed Effects Models in S and S-Plus. Springer, New York.
53. R Development Core Team (2008) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
54. Rasbash J, Steele F, Browne W, Prosser B, (2005) A User's Guide to MLwiN-Version 2.0. Centre for Multilevel Modelling, University of Bristol, London.
55. Reid JM, Arcese P, Keller LF, Elliott KH, Sampson L, Hasselquist D, (2007) Inbreeding effects on immune response in free-living song sparrows (Melospiza melodia). Proceedings of the Royal Society B-Biological Sciences, 274, 697-706. (Pubitemid 47056785)
56. Richardson DS, Komdeur J, Burke T, (2004) Inbreeding in the seychelles warbler: environment-dependent maternal effects. Evolution, 58, 2037-2048. (Pubitemid 39348504)
57. Rioux-Paquette E, Festa-Bianchet M, Coltman DW, (2011) Sex-differential effects of inbreeding on overwinter survival, birth date and mass of bighorn lambs. Journal of Evolutionary Biology, 24, 121-131.
58. Rossiter SJ, Jones G, Ransome RD, Barratt EM, (2001) Outbreeding increases offspring survival in wild greater horseshoe bats (Rhinolophus ferrumequinum). Proceedings of the Royal Society of London Series B-Biological Sciences, 268, 1055-1061. (Pubitemid 32500479)
59. Saccheri IJ, Lloyd HD, Helyar SJ, Brakefield PM, (2005) Inbreeding uncovers fundamental differences in the genetic load affecting male and female fertility in a butterfly. Proceedings of the Royal Society of London Series B-Biological Sciences, 272, 39-46.
60. Slate J, David P, Dodds KG, et al. (2004) Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity, 93, 255-265. (Pubitemid 39147529)
61. Smallegange IM, Fiedler W, Koppen U, Geiter O, Bairlein F, (2010) Tits on the move: exploring the impact of environmental change on blue tit and great tit migration distance. Journal of Animal Ecology, 79, 350-357.
62. Svensson L, (1992) Identification Guide to European Passerine Birds, 4th edn. Stockholm.
63. Szulkin M, Bierne N, David P, (2010) Heterozygosity-fitness correlations: a time for reappraisal. Evolution, 64, 1202-1217.
64. Taylor SS, Sardell RJ, Reid JM, et al. (2010) Inbreeding coefficient and heterozygosity-fitness correlations in unhatched and hatched song sparrow nestmates. Molecular Ecology, 19, 4454-4461.
65. Valcu M, Kempenaers B, (2008) Causes and consequences of breeding dispersal and divorce in a blue tit, Cyanistes caeruleus, population. Animal Behaviour, 75, 1949-1963.
66. van de Pol MV, Wright J, (2009) A simple method for distinguishing within- versus between-subject effects using mixed models. Animal Behaviour, 77, 753-758.
67. Vasemagi A, Nilsson J, Primmer CR, (2005) Expressed sequence tag-linked microsatellites as a source of gene-associated polymorphisms for detecting signatures of divergent selection in Atlantic salmon (Salmo salar L.). Molecular Biology and Evolution, 22, 1067-1076. (Pubitemid 40471419)
68. Warren WC, Clayton DF, Ellegren H, et al. (2010) The genome of a songbird. Nature, 464, 757-762.