QTL and quantitative genetic analysis of beak morphology reveals patterns of standing genetic variation in an estrildid finch

Molecular Ecology

Volumn 21, Issue 15, 2012, Pages 3704-3717

  Knief, Ulrich ^a   Schielzeth, Holger ^b   Kempenaers, Bart ^a   Ellegren, Hans ^b   Forstmeier, Wolfgang ^a  

^a MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

candidate genes; G matrices; genetic correlations; QTL mapping; quantitative genetics; sexual dimorphism; Taeniopygia guttata; zebra finch

Indexed keywords

ANIMAL; ARTICLE; BEAK; CHROMOSOME MAP; FEMALE; FINCH; GENETIC LINKAGE; GENETIC VARIABILITY; GENETICS; HISTOLOGY; MALE; PHENOTYPE; QUANTITATIVE TRAIT LOCUS; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; BEAK; CHROMOSOME MAPPING; FEMALE; FINCHES; GENETIC LINKAGE; GENETIC VARIATION; MALE; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI;

AVES; ESTRILDIDAE; TAENIOPYGIA GUTTATA;

EID: 84864279335     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2012.05661.x     Document Type: Article

References (69)

1. Abzhanov A, Tabin CJ, (2004) Shh and Fgf8 act synergistically to drive cartilage outgrowth during cranial development. Developmental Biology, 273, 134-148. (Pubitemid 39078372)
2. Abzhanov A, Protas M, Grant BR, Grant PR, Tabin CJ, (2004) Bmp4 and morphological variation of beaks in Darwin's finches. Science, 305, 1462-1465. (Pubitemid 39167665)
3. Abzhanov A, Kuo WP, Hartmann C, et al. (2006) The calmodulin pathway and evolution of elongated beak morphology in Darwin's finches. Nature, 442, 563-567. (Pubitemid 44167914)
4. Åkesson M, Bensch S, Hasselquist D, Tarka M, Hansson B, (2008) Estimating heritabilities and genetic correlations: comparing the 'animal model' with parent-offspring regression using data from a natural population. PLoS One, 3, e1739.
5. Backström N, Forstmeier W, Schielzeth H, et al. (2010) The recombination landscape of the zebra finch Taeniopygia guttata genome. Genome Research, 20, 485-495.
6. Badyaev AV, (2010) The beak of the other finch: coevolution of genetic covariance structure and developmental modularity during adaptive evolution. Philosophical Transactions of the Royal Society B-Biological Sciences, 365, 1111-1126.
7. Beavis WD, (1998) QTL analysis: power, precision, and accuracy. In: Molecular Dissection of Complex Traits (ed., Paterson AH,), pp. 145-162. CRC Press, Boca Raton, Florida.
8. Cheung VG, Spielman RS, (2009) Genetics of human gene expression: mapping DNA variants that influence gene expression. Nature Reviews Genetics, 10, 595-604.
9. Cheung VG, Nayak RR, Wang IXR, et al. (2010) Polymorphic cis- and trans-regulation of human gene expression. Plos Biology, 8, e1000480.
10. Collins SA, ten Cate C, (1996) Does beak colour affect female preference in zebra finches? Animal Behaviour, 52, 105-112.
11. Darwin C, (1859) On the Origin of Species by Means of Natural Selection. John Murray, London.
12. Dupuis J, Siegmund D, (1999) Statistical methods for mapping quantitative trait loci from a dense set of markers. Genetics, 151, 373-386. (Pubitemid 29031902)
13. Falconer D, Mackay T, (1996) Introduction to Quantitative Genetics. Longmann, Harlow, UK.
14. Fan JB, Oliphant A, Shen R, et al. (2003) Highly parallel SNP genotyping. Cold Spring Harbor Symposia on Quantitative Biology, 68, 69-78. (Pubitemid 38955554)
15. Flint J, Mackay TFC, (2009) Genetic architecture of quantitative traits in mice, flies, and humans. Genome Research, 19, 723-733.
16. Forstmeier W, (2011) Women have relatively larger brains than men: a comment on the misuse of general linear models in the study of sexual dimorphism. Anatomical Record, 294, 1856-1863.
17. Forstmeier W, Birkhead TR, (2004) Repeatability of mate choice in the zebra finch: consistency within and between females. Animal Behaviour, 68, 1017-1028. (Pubitemid 39379532)
18. Forstmeier W, Schielzeth H, (2011) Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner's curse. Behavioral Ecology and Sociobiology, 65, 47-55.
19. Forstmeier W, Leisler B, Kempenaers B, (2001) Bill morphology reflects female independence from male parental help. Proceedings of the Royal Society B-Biological Science, 268, 1583-1588. (Pubitemid 32730414)
20. Forstmeier W, Segelbacher G, Mueller JC, Kempenaers B, (2007) Genetic variation and differentiation in captive and wild zebra finches (Taeniopygia guttata). Molecular Ecology, 16, 4039-4050. (Pubitemid 47481041)
21. Fox W, (1952) Behavioral and evolutionary significance of the abnormal growth of beaks of birds. Condor, 54, 160-162.
22. George AW, Visscher PM, Haley CS, (2000) Mapping quantitative trait loci in complex pedigrees: a two-step variance component approach. Genetics, 156, 2081-2092. (Pubitemid 32001265)
23. Gilmour AR, Gogel BJ, Cullis BR, Thompson R, (2009) ASReml User Guide. VSN International, Hemel Hempstead, UK.
24. Göring HHH, Terwilliger JD, Blangero J, (2001) Large upward bias in estimation of locus-specific effects from genomewide scans. American Journal of Human Genetics, 69, 1357-1369. (Pubitemid 33124216)
25. Gosler AG, (1987) Pattern and process in the bill morphology of the great tit Parus major. Ibis, 129, 451-476. (Pubitemid 19318914)
26. Grant PR, (1999) Ecology and Evolution of Darwin's Finches. Princeton University Press, Princeton, New Jersey.
27. Grant PR, Grant BR, (2002) Unpredictable evolution in a 30-year study of Darwin's finches. Science, 296, 707-711. (Pubitemid 34441992)
28. Groeneveld E, Kovač M, Mielenz N, (2008) VCE User's Guide and Reference Manual. Version 6.0. Institute of Farm Animal Genetics, Friedrich Loeffler Institute (FLI), Mariensee, Germany.
29. Hadfield JD, Nutall A, Osorio D, Owens IPF, (2007) Testing the phenotypic gambit: phenotypic, genetic and environmental correlations of colour. Journal of Evolutionary Biology, 20, 549-557.
30. Hansen TF, Houle D, (2008) Measuring and comparing evolvability and constraint in multivariate characters. Journal of Evolutionary Biology, 21, 1201-1219.
31. Hernandez-Sanchez J, Grunchec JA, Knott S, (2009) A web application to perform linkage disequilibrium and linkage analyses on a computational grid. Bioinformatics, 25, 1377-1383.
32. Herrel A, Soons J, Aerts P, et al. (2010) Adaptation and function of the bills of Darwin's finches: divergence by feeding type and sex. Emu, 110, 39-47.
33. Houle D, (1992) Comparing evolvability and variability of quantitative traits. Genetics, 130, 195-204.
34. Hu D, Marcucio RS, Helms JA, (2003) A zone of frontonasal ectoderm regulates patterning and growth in the face. Development, 130, 1749-1758. (Pubitemid 36575903)
35. Keller LF, Grant PR, Grant BR, Petren K, (2001) Heritability of morphological traits in Darwin's Finches: misidentified paternity and maternal effects. Heredity, 87, 325-336. (Pubitemid 33136803)
36. Lander ES, Botstein D, (1989) Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics, 121, 185-199.
37. Lander E, Kruglyak L, (1995) Genetic dissection of complex traits: guidelines for interpreting and reporting linkage results. Nature Genetics, 11, 241-247.
38. Lee SH, Fu KK, Hui JN, Richman JM, (2001) Noggin and retinoic acid transform the identity of avian facial prominences. Nature, 414, 909-912. (Pubitemid 34024741)
39. Mallarino R, Grant PR, Grant BR, et al. (2011) Two developmental modules establish 3D beak-shape variation in Darwin's finches. Proceedings of the National Academy of Sciences USA, 108, 4057-4062.
40. Matthysen E, (1989) Seasonal variation in bill morphology of nuthatches Sitta europaea- dietary adaptations or consequences? Ardea, 77, 117-125.
41. Nakagawa S, Cuthill IC, (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biological Reviews, 82, 591-605. (Pubitemid 47609922)
42. Pavlicev M, Kenney-Hunt JP, Norgard EA, et al. (2008) Genetic variation in pleiotropy: differential epistasis as a source of variation in the allometric relationship between long bone lengths and body weight. Evolution, 62, 199-213.
43. Podos J, (2001) Correlated evolution of morphology and vocal signal structure in Darwin's finches. Nature, 409, 185-188. (Pubitemid 32146168)
44. Podos J, Nowicki S, (2004) Beaks, adaptation, and vocal evolution in Darwin's finches. BioScience, 54, 501-510. (Pubitemid 38751836)
45. Pong-Wong R, George AW, Woolliams JA, Haley CS, (2001) A simple and rapid method for calculating identity-by-descent matrices using multiple markers. Genetics Selection Evolution, 33, 453-471. (Pubitemid 33043096)
46. Price TD, Grant PR, (1984) Life history traits and natural selection for small body size in a population of Darwin's finches. Evolution, 38, 483-494. (Pubitemid 16274044)
47. R Development Core Team (2011) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
48. Radford AN, Du Plessis MA, (2003) Bill dimorphism and foraging niche partitioning in the green woodhoopoe. Journal of Animal Ecology, 72, 258-269. (Pubitemid 36420964)
49. Riley CM, Smith KG, (1992) Sexual dimorphism and foraging behavior of emerald toucanets Aulacorhynchus prasinus in Costa Rica. Ornis Scandinavica, 23, 459-466.
50. Ryan MJ, (1998) Sexual selection, receiver biases, and the evolution of sex differences. Science, 281, 1999-2003. (Pubitemid 28475482)
51. Schielzeth H, Kempenaers B, Ellegren H, Forstmeier W, (2011) Data from: QTL linkage mapping of zebra finch beak color shows an oligogenic control of a sexually selected trait. Dryad Digital Repository, doi:10.5061/dryad.r044b.
52. Schielzeth H, Forstmeier W, Kempenaers B, Ellegren H, (2012a) QTL linkage mapping of wing length in zebra finch using genome-wide single nucleotide polymorphisms markers. Molecular Ecology, 21, 329-339.
53. Schielzeth H, Kempenaers B, Ellegren H, Forstmeier W, (2012b) QTL linkage mapping of zebra finch beak color shows an oligogenic control of a sexually selected trait. Evolution, 66, 18-30.
54. Schneider RA, Hu D, Rubenstein JL, Maden M, Helms JA, (2001) Local retinoid signaling coordinates forebrain and facial morphogenesis by maintaining FGF8 and SHH. Development, 128, 2755-2767. (Pubitemid 32701004)
55. Selander RK, (1966) Sexual dimorphism and differential niche utilization in birds. Condor, 68, 113-151.
56. Smith JNM, Arcese P, Schluter D, (1986) Song sparrows grow and shrink with age. Auk, 103, 210-212.
57. Song Y, Hui JN, Fu KK, Richman JM, (2004) Control of retinoic acid synthesis and FGF expression in the nasal pit is required to pattern the craniofacial skeleton. Developmental Biology, 276, 313-329. (Pubitemid 39592396)
58. SPSS Inc. (2009) PASW Statistics for Windows, Rel. 18.0.0. SPSS Inc., Chicago, Illinois.
59. Svensson L, (1992) Identification Guide to European Passerines, 4th edn. L. Svensson, Stockholm.
60. Takahasi KR, Matsuo T, Takano-Shimizu-Kouno T, (2011) Two types of cis-trans compensation in the evolution of transcriptional regulation. Proceedings of the National Academy of Sciences USA, 108, 15276-15281.
61. Tschirren B, Postma E, (2010) Quantitative genetics research in zebra finches: where we are and where to go. Emu, 110, 268-278.
62. Veyrieras JB, Kudaravalli S, Kim SY, et al. (2008) High-resolution mapping of expression-QTLs yields insight into human gene regulation. Plos Genetics, 4, e1000214.
63. Warren WC, Clayton DF, Ellegren H, et al. (2010) The genome of a songbird. Nature, 464, 757-762.
64. Weigensberg I, Roff DA, (1996) Natural heritabilities: Can they be reliably estimated in the laboratory? Evolution, 50, 2149-2157.
65. Wray GA, (2007) The evolutionary significance of cis-regulatory mutations. Nature Reviews Genetics, 8, 206-216.
66. Wu P, Jiang TX, Suksaweang S, Widelitz RB, Chuong CM, (2004) Molecular shaping of the beak. Science, 305, 1465-1466. (Pubitemid 39167666)
67. Wu P, Jiang TX, Shen JY, Widelitz RB, Chuong CM, (2006) Morphoregulation of avian beaks: comparative mapping of growth zone activities and morphological evolution. Developmental Dynamics, 235, 1400-1412. (Pubitemid 43843921)
68. Zann RA, (1996) The Zebra Finch: A Synthesis of Field and Laboratory Studies. Oxford University Press, USA.
69. Ziegler A, König IR, (2006) A Statistical Approach to Genetic Epidemiology: Concepts and Applications. John Wiley & Sons, Incorporated, Weinheim, Germany.