Heterozygosity-fitness correlations in zebra finches: microsatellite markers can be better than their reputation

Forstmeier W, Schielzeth H, Mueller JC, Ellegren H, Kempenaers B (2012)
Molecular Ecology 21(13): 3237-3249.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
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Autor*in
Forstmeier, W.; Schielzeth, HolgerUniBi ; Mueller, J. C.; Ellegren, H.; Kempenaers, B.
Abstract / Bemerkung
Numerous studies have reported associations between heterozygosity in microsatellite markers and fitness-related traits (heterozygosity–fitness correlations, HFCs). However,it has often been questioned whether HFCs reflect general inbreeding depression, because a small panel of microsatellite markers does not reflect very well an individual’s inbreeding coefficient (F) as calculated from a pedigree. Here, we challenge this prevailing view. Because of chance events during Mendelian segregation, an individual’s realized proportion of the genome that is identical by descent (IBD) may substantially deviate from the pedigree-based expectation (i.e. F). This Mendelian noise may result in a weak correlation between F and multi-locus heterozygosity, but this does not imply that multi-locus heterozygosity is a bad estimator of realized IBD. We examined correlations between 11 fitness-related traits measured in up to 1192 captive zebra finches and three measures of inbreeding: (i) heterozygosity across 11 microsatellite markers, (ii) heterozygosity across 1359 single-nucleotide polymorphism (SNP) markers and (iii) F, based on a 5th-generation pedigree. All 11 phenotypic traits showed positive relationships with measures of heterozygosity, especially traits that are most closely related to fitness. Remarkably, the small panel of microsatellite markers produced equally strong HFCs as the large panel of SNP markers. Both marker-based approaches produced stronger correlations with phenotypes than the pedigree-based F, and this did not seem to result from the shortness of our pedigree. We argue that a small panel of microsatellites with high allelic richness may better reflect an individual’s realized IBD than previously appreciated, especially in species like the zebra finch, where much of the genome is inherited in large blocks that rarely experience cross-over during meiosis.
Erscheinungsjahr
2012
Zeitschriftentitel
Molecular Ecology
Band
21
Ausgabe
13
Seite(n)
3237-3249
ISSN
0962-1083
Page URI
https://pub.uni-bielefeld.de/record/2496150

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Forstmeier W, Schielzeth H, Mueller JC, Ellegren H, Kempenaers B. Heterozygosity-fitness correlations in zebra finches: microsatellite markers can be better than their reputation. Molecular Ecology. 2012;21(13):3237-3249.
Forstmeier, W., Schielzeth, H., Mueller, J. C., Ellegren, H., & Kempenaers, B. (2012). Heterozygosity-fitness correlations in zebra finches: microsatellite markers can be better than their reputation. Molecular Ecology, 21(13), 3237-3249. doi:10.1111/j.1365-294X.2012.05593.x
Forstmeier, W., Schielzeth, H., Mueller, J. C., Ellegren, H., and Kempenaers, B. (2012). Heterozygosity-fitness correlations in zebra finches: microsatellite markers can be better than their reputation. Molecular Ecology 21, 3237-3249.
Forstmeier, W., et al., 2012. Heterozygosity-fitness correlations in zebra finches: microsatellite markers can be better than their reputation. Molecular Ecology, 21(13), p 3237-3249.
W. Forstmeier, et al., “Heterozygosity-fitness correlations in zebra finches: microsatellite markers can be better than their reputation”, Molecular Ecology, vol. 21, 2012, pp. 3237-3249.
Forstmeier, W., Schielzeth, H., Mueller, J.C., Ellegren, H., Kempenaers, B.: Heterozygosity-fitness correlations in zebra finches: microsatellite markers can be better than their reputation. Molecular Ecology. 21, 3237-3249 (2012).
Forstmeier, W., Schielzeth, Holger, Mueller, J. C., Ellegren, H., and Kempenaers, B. “Heterozygosity-fitness correlations in zebra finches: microsatellite markers can be better than their reputation”. Molecular Ecology 21.13 (2012): 3237-3249.

77 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Heterozygosity at neutral and immune loci is not associated with neonatal mortality due to microbial infection in Antarctic fur seals.
Litzke V, Ottensmann M, Forcada J, Heitzmann L, Ivan Hoffman J., Ecol Evol 9(14), 2019
PMID: 31380066
Genomic consequences of intensive inbreeding in an isolated wolf population.
Kardos M, Åkesson M, Fountain T, Flagstad Ø, Liberg O, Olason P, Sand H, Wabakken P, Wikenros C, Ellegren H., Nat Ecol Evol 2(1), 2018
PMID: 29158554
Genetic diversity and parasite facilitated establishment of the invasive signal crayfish (Pacifastacus leniusculus) in Great Britain.
Robinson CV, Garcia de Leaniz C, James J, Cable J, Orozco-terWengel P, Consuegra S., Ecol Evol 8(18), 2018
PMID: 30377493
Genetic diversity in fishes is influenced by habitat type and life-history variation.
Martinez AS, Willoughby JR, Christie MR., Ecol Evol 8(23), 2018
PMID: 30598796
Meiotic recombination shapes precision of pedigree- and marker-based estimates of inbreeding.
Knief U, Kempenaers B, Forstmeier W., Heredity (Edinb) 118(3), 2017
PMID: 27804967
The inbreeding strategy of a solitary primate, Microcebus murinus.
Huchard E, Schliehe-Diecks S, Kappeler PM, Kraus C., J Evol Biol 30(1), 2017
PMID: 27790777
Inbreeding avoidance and female mate choice shape reproductive skew in capuchin monkeys (Cebus capucinus imitator).
Wikberg EC, Jack KM, Fedigan LM, Campos FA, Yashima AS, Bergstrom ML, Hiwatashi T, Kawamura S., Mol Ecol 26(2), 2017
PMID: 27797426
Low incidence of inbreeding in a long-lived primate population isolated for 75 years.
Widdig A, Muniz L, Minkner M, Barth Y, Bley S, Ruiz-Lambides A, Junge O, Mundry R, Kulik L., Behav Ecol Sociobiol 71(1), 2017
PMID: 28018027
Pedigree-based inbreeding coefficient explains more variation in fitness than heterozygosity at 160 microsatellites in a wild bird population.
Nietlisbach P, Keller LF, Camenisch G, Guillaume F, Arcese P, Reid JM, Postma E., Proc Biol Sci 284(1850), 2017
PMID: 28250184
Testing the phenotype-linked fertility hypothesis in the presence and absence of inbreeding.
Forstmeier W, Ihle M, Opatová P, Martin K, Knief U, Albrechtová J, Albrecht T, Kempenaers B., J Evol Biol 30(5), 2017
PMID: 28278362
Population demography and heterozygosity-fitness correlations in natural guppy populations: An examination using sexually selected fitness traits.
Grueber CE, Fitzpatrick JL, Devigili A, Gasparini C, Ramnarine IW, Evans JP., Mol Ecol 26(18), 2017
PMID: 28734054
Sexual selection on male body size, genital length and heterozygosity: Consistency across habitats and social settings.
Head ML, Kahn AT, Henshaw JM, Keogh JS, Jennions MD., J Anim Ecol 86(6), 2017
PMID: 28815592
Host heterozygosity and genotype rarity affect viral dynamics in an avian subspecies complex.
Eastwood JR, Ribot RFH, Rollins LA, Buchanan KL, Walder K, Bennett ATD, Berg ML., Sci Rep 7(1), 2017
PMID: 29042596
No mutual mate choice for quality in zebra finches: Time to question a widely held assumption.
Wang D, Forstmeier W, Kempenaers B., Evolution 71(11), 2017
PMID: 28857165
Cryptic female choice enhances fertilization success and embryo survival in chinook salmon.
Rosengrave P, Montgomerie R, Gemmell N., Proc Biol Sci 283(1827), 2016
PMID: 27009221
Evidence of the phenotypic expression of a lethal recessive allele under inbreeding in a wild population of conservation concern.
Trask AE, Bignal EM, McCracken DI, Monaghan P, Piertney SB, Reid JM., J Anim Ecol 85(4), 2016
PMID: 26996516
Genomic analysis reveals depression due to both individual and maternal inbreeding in a free-living mammal population.
Bérénos C, Ellis PA, Pilkington JG, Pemberton JM., Mol Ecol 25(13), 2016
PMID: 27135155
High-throughput sequencing and graph-based cluster analysis facilitate microsatellite development from a highly complex genome.
Shah AB, Schielzeth H, Albersmeier A, Kalinowski J, Hoffman JI., Ecol Evol 6(16), 2016
PMID: 27547349
A genetic assessment of the English bulldog.
Pedersen NC, Pooch AS, Liu H., Canine Genet Epidemiol 3(), 2016
PMID: 27478618
Genetic rescue in a severely inbred wolf population.
Åkesson M, Liberg O, Sand H, Wabakken P, Bensch S, Flagstad Ø., Mol Ecol 25(19), 2016
PMID: 27497431
Fitness consequences of polymorphic inversions in the zebra finch genome.
Knief U, Hemmrich-Stanisak G, Wittig M, Franke A, Griffith SC, Kempenaers B, Forstmeier W., Genome Biol 17(1), 2016
PMID: 27687629
Understanding Inbreeding Depression, Purging, and Genetic Rescue.
Hedrick PW, Garcia-Dorado A., Trends Ecol Evol 31(12), 2016
PMID: 27743611
Genomics advances the study of inbreeding depression in the wild.
Kardos M, Taylor HR, Ellegren H, Luikart G, Allendorf FW., Evol Appl 9(10), 2016
PMID: 27877200
Revealing hidden species diversity in closely related species using nuclear SNPs, SSRs and DNA sequences - a case study in the tree genus Milicia.
Daïnou K, Blanc-Jolivet C, Degen B, Kimani P, Ndiade-Bourobou D, Donkpegan AS, Tosso F, Kaymak E, Bourland N, Doucet JL, Hardy OJ., BMC Evol Biol 16(1), 2016
PMID: 27903256
Three Molecular Markers Show No Evidence of Population Genetic Structure in the Gouldian Finch (Erythrura gouldiae).
Bolton PE, West AJ, Cardilini AP, Clark JA, Maute KL, Legge S, Brazill-Boast J, Griffith SC, Rollins LA., PLoS One 11(12), 2016
PMID: 27936082
Reduced microsatellite heterozygosity does not affect natal dispersal in three contrasting roe deer populations.
Vanpé C, Debeffe L, Hewison AJM, Quéméré E, Lemaître JF, Galan M, Amblard B, Klein F, Cargnelutti B, Capron G, Merlet J, Warnant C, Gaillard JM., Oecologia 177(3), 2015
PMID: 25388875
Quantifying inbreeding avoidance through extra-pair reproduction.
Reid JM, Arcese P, Keller LF, Germain RR, Duthie AB, Losdat S, Wolak ME, Nietlisbach P., Evolution 69(1), 2015
PMID: 25346331
Quantifying realized inbreeding in wild and captive animal populations.
Knief U, Hemmrich-Stanisak G, Wittig M, Franke A, Griffith SC, Kempenaers B, Forstmeier W., Heredity (Edinb) 114(4), 2015
PMID: 25585923
Differential effects of genetic vs. environmental quality in Drosophila melanogaster suggest multiple forms of condition dependence.
Bonduriansky R, Mallet MA, Arbuthnott D, Pawlowsky-Glahn V, Egozcue JJ, Rundle HD., Ecol Lett 18(4), 2015
PMID: 25649176
Heterozygosity-fitness correlations in a declining seabird population.
Velando A, Barros Á, Moran P., Mol Ecol 24(5), 2015
PMID: 25626726
Measuring individual inbreeding in the age of genomics: marker-based measures are better than pedigrees.
Kardos M, Luikart G, Allendorf FW., Heredity (Edinb) 115(1), 2015
PMID: 26059970
Local Heterozygosity Effects on Nestling Growth and Condition in the Great Cormorant.
Minias P, Wojczulanis-Jakubas K, Rutkowski R, Kaczmarek K., Evol Biol 42(4), 2015
PMID: 26586922
The effect of genetic bottlenecks and inbreeding on the incidence of two major autoimmune diseases in standard poodles, sebaceous adenitis and Addison's disease.
Pedersen NC, Brucker L, Tessier NG, Liu H, Penedo MC, Hughes S, Oberbauer A, Sacks B., Canine Genet Epidemiol 2(), 2015
PMID: 26401342
Context-dependent associations between heterozygosity and immune variation in a wild carnivore.
Brock PM, Goodman SJ, Hall AJ, Cruz M, Acevedo-Whitehouse K., BMC Evol Biol 15(), 2015
PMID: 26537228
Spatial Isolation and Temporal Variation in Fitness and Condition Facilitate Divergence in a Migratory Divide.
Hermes C, Mettler R, Santiago-Alarcon D, Segelbacher G, Schaefer HM., PLoS One 10(12), 2015
PMID: 26656955
Advancing avian behavioral neuroendocrinology through genomics.
Clayton DF, London SE., Front Neuroendocrinol 35(1), 2014
PMID: 24113222
Estimating genome-wide heterozygosity: effects of demographic history and marker type.
Miller JM, Malenfant RM, David P, Davis CS, Poissant J, Hogg JT, Festa-Bianchet M, Coltman DW., Heredity (Edinb) 112(3), 2014
PMID: 24149650
Heterozygosity and orange coloration are associated in the guppy (Poecilia reticulata).
Herdegen M, Dudka K, Radwan J., J Evol Biol 27(1), 2014
PMID: 24329722
High-throughput sequencing reveals inbreeding depression in a natural population.
Hoffman JI, Simpson F, David P, Rijks JM, Kuiken T, Thorne MA, Lacy RC, Dasmahapatra KK., Proc Natl Acad Sci U S A 111(10), 2014
PMID: 24586051
Heterozygosity-fitness correlations in a wild mammal population: accounting for parental and environmental effects.
Annavi G, Newman C, Buesching CD, Macdonald DW, Burke T, Dugdale HL., Ecol Evol 4(12), 2014
PMID: 25360289
Genetic depletion at adaptive but not neutral loci in an endangered bird species.
Hartmann SA, Schaefer HM, Segelbacher G., Mol Ecol 23(23), 2014
PMID: 25345968
Sex chromosome linked genetic variance and the evolution of sexual dimorphism of quantitative traits.
Husby A, Schielzeth H, Forstmeier W, Gustafsson L, Qvarnström A., Evolution 67(3), 2013
PMID: 23461313
Has the inbreeding load for a condition-dependent sexual signalling trait been purged in insular lizard populations?
Runemark A, Hansson B, Ljungqvist M, Brydegaard M, Svensson EI., Mol Ecol 22(5), 2013
PMID: 23294127
Investigation of individual heterozygosity correlated to growth traits in Tongshan Black-boned goat.
Han YG, Liu GQ, Jiang XP, Liang GM, He CB, Wang DW, Wu Y, Xiang XL, Hu J, Peng YQ., Mol Biol Rep 40(11), 2013
PMID: 24057243
Extra-group mating increases inbreeding risk in a cooperatively breeding bird.
Harrison XA, York JE, Cram DL, Young AJ., Mol Ecol 22(22), 2013
PMID: 24118639
Heterozygosity is linked to the costs of immunity in nestling great tits (Parus major).
Voegeli B, Saladin V, Wegmann M, Richner H., Ecol Evol 3(14), 2013
PMID: 24363906

46 References

Daten bereitgestellt von Europe PubMed Central.

The influence of parental relatedness on reproductive success
Amos, Proceedings of the Royal Society B-Biological Sciences 268(), 2001
What should we weigh to estimate heterozygosity, alleles or loci?
Aparicio JM, Ortego J, Cordero PJ., Mol. Ecol. 15(14), 2006
PMID: 17107491
The recombination landscape of the zebra finch Taeniopygia guttata genome.
Backstrom N, Forstmeier W, Schielzeth H, Mellenius H, Nam K, Bolund E, Webster MT, Ost T, Schneider M, Kempenaers B, Ellegren H., Genome Res. 20(4), 2010
PMID: 20357052
Does heterozygosity estimate inbreeding in real populations?
Balloux F, Amos W, Coulson T., Mol. Ecol. 13(10), 2004
PMID: 15367117
Selection for heterozygosity gives hope to a wild population of inbred wolves.
Bensch S, Andren H, Hansson B, Pedersen HC, Sand H, Sejberg D, Wabakken P, Akesson M, Liberg O., PLoS ONE 1(), 2006
PMID: 17183704
Early effect of inbreeding as revealed by microsatellite analyses on Ostrea edulis larvae.
Bierne N, Launey S, Naciri-Graven Y, Bonhomme F., Genetics 148(4), 1998
PMID: 9560403
Inbreeding depression of sexually selected traits and attractiveness in the zebra finch
Bolund, Animal Behaviour 79(), 2010
A quantitative review of heterozygosity-fitness correlations in animal populations.
Chapman JR, Nakagawa S, Coltman DW, Slate J, Sheldon BC., Mol. Ecol. 18(13), 2009
PMID: 19500255
Microsatellite measures of inbreeding: a meta-analysis.
Coltman DW, Slate J., Evolution 57(5), 2003
PMID: 12836816
Parasite-mediated selection against inbred Soay sheep in a free-living, island population.
Coltman DW, Pilkington JG, Smith JA, Pemberton JM., Evolution 53(4), 1999
PMID: IND22030991
Microsatellites reveal heterosis in red deer
Coulson, Proceedings of the Royal Society B-Biological Sciences 265(), 1998
Heterozygosity-fitness correlations: new perspectives on old problems.
David P., Heredity (Edinb) 80 ( Pt 5)(), 1998
PMID: 9650277
On the genealogy of a population of biparental individuals.
Derrida B, Manrubia SC, Zanette DH., J. Theor. Biol. 203(3), 2000
PMID: 10716910
Maternal effects influence the sexual behavior of sons and daughters in the zebra finch.
Forstmeier W, Coltman DW, Birkhead TR., Evolution 58(11), 2004
PMID: 15612299
Development of polymorphic microsatellite markers for the zebra finch (Taeniopygia guttata)
FORSTMEIER W, SCHIELZETH H, SCHNEIDER M, KEMPENAERS B., Mol. Ecol. Notes 7(6), 2007
PMID: IND43974441
Genetic variation and differentiation in captive and wild zebra finches (Taeniopygia guttata).
Forstmeier W, Segelbacher G, Mueller JC, Kempenaers B., Mol. Ecol. 16(19), 2007
PMID: 17894758
A polymorphism in the oestrogen receptor gene explains covariance between digit ratio and mating behaviour
Forstmeier, Proceedings of the Royal Society B-Biological Sciences 277(), 2010
Female extrapair mating behavior can evolve via indirect selection on males.
Forstmeier W, Martin K, Bolund E, Schielzeth H, Kempenaers B., Proc. Natl. Acad. Sci. U.S.A. 108(26), 2011
PMID: 21670288
The correlation between inbreeding and fitness: does allele size matter?
Goudet, Trends in Ecology and Evolution 17(), 2002
On the correlation between heterozygosity and fitness in natural populations.
Hansson B, Westerberg L., Mol. Ecol. 11(12), 2002
PMID: 12453232
Does linkage disequilibrium generate heterozygosity-fitness correlations in great reed warblers?
Hansson B, Westerdahl H, Hasselquist D, Akesson M, Bensch S., Evolution 58(4), 2004
PMID: 15154561
Enhanced genetic maps from family-based disease studies: population-specific comparisons
He, BMC Medical Genetics 12(), 2011

Kinghorn, 2010
Research on inbreeding in the 'omic' era.
Kristensen TN, Pedersen KS, Vermeulen CJ, Loeschcke V., Trends Ecol. Evol. (Amst.) 25(1), 2009
PMID: 19733933
Estimation of the inbreeding coefficient through use of genomic data.
Leutenegger AL, Prum B, Genin E, Verny C, Lemainque A, Clerget-Darpoux F, Thompson EA., Am. J. Hum. Genet. 73(3), 2003
PMID: 12900793
Neutral locus heterozygosity, inbreeding, and survival in Darwin's ground finches (Geospiza fortis and G. scandens).
Markert JA, Grant PR, Grant BR, Keller LF, Coombs JL, Petren K., Heredity (Edinb) 92(4), 2004
PMID: 14735140
Measuring inbreeding depression in the wild: the old ways are the best.
Pemberton J., Trends Ecol. Evol. (Amst.) 19(12), 2004
PMID: 16701322
Wild pedigrees: the way forward
Pemberton, Proceedings of the Royal Society B-Biological Sciences 275(), 2008

R, 2011
GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism
Raymond, Journal of Heredity 86(), 1995
Heritability of and early environment effects on variation in mating preferences.
Schielzeth H, Bolund E, Forstmeier W., Evolution 64(4), 2009
PMID: 19895552
QTL linkage mapping of zebra finch beak colour shows an oligogenic control of a sexually selected trait
Schielzeth, Evolution 68(), 2012
Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data.
Slate J, David P, Dodds KG, Veenvliet BA, Glass BC, Broad TE, McEwan JC., Heredity (Edinb) 93(3), 2004
PMID: 15254488
How many SNPs are enough?
Smouse PE., Mol. Ecol. 19(7), 2010
PMID: 20456228

Sokal, 1995
The distribution of the fraction of the genome identical by descent in finite random mating populations
Stam, Genetical Research 35(), 1980
Inbreeding coefficient and heterozygosity-fitness correlations in unhatched and hatched song sparrow nestmates.
Taylor SS, Sardell RJ, Reid JM, Bucher T, Taylor NG, Arcese P, Keller LF., Mol. Ecol. 19(20), 2010
PMID: 20854411
Heterosis, marker mutational processes and population inbreeding history.
Tsitrone A, Rousset F, David P., Genetics 159(4), 2001
PMID: 11779819
Developmental stress and female mate choice behaviour in the zebra finch
Woodgate, Animal Behaviour 79(), 2010

Zann, 1996
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