Candidate genes for colour and vision exhibit signals of selection across the pied flycatcher (Ficedula hypoleuca) breeding range

Heredity

Volumn 108, Issue 4, 2012, Pages 431-440

  Lehtonen, P K ^a   Laaksonen, T ^a   Artemyev, A V ^b   Belskii, E ^c   Berg, P R ^d,o   Both, C ^e   Buggiotti, L ^a,q   Bures S ^f   Burgess, M D ^g   Bushuev, A V ^h   Krams, I ^a,i   Moreno, J ^j   Magi M ^k   Nord, A ^l   Potti, J ^m   Ravussin, P A ⁿ   Sirkia P M ^a   Saetre G P ^o   Winkel, W ^p   Primmer, C R ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b INSTITUTE OF BIOLOGY   (Russian Federation)

^c INSTITUTE OF PLANT AND ANIMAL ECOLOGY   (Russian Federation)

^d NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^e UNIVERSITY OF GRONINGEN   (Netherlands)

^f PALACKÝ UNIVERSITY   (Czech Republic)

^g UNIVERSITY OF EXETER   (United Kingdom)

^h MOSCOW STATE UNIVERSITY   (Russian Federation)

ⁱ DAUGAVPILS UNIVERSITY   (Latvia)

^j MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

^k UNIVERSITY OF TARTU   (Estonia)

^l LUND UNIVERSITY   (Sweden)

^m DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

ⁿ Institute of Avian Research ^*  (Switzerland)

^o UNIVERSITY OF OSLO   (Norway)

^p INSTITUTE OF AVIAN RESEARCH VOGELWARTE HELGOLAND   (Germany)

^q UNIVERSITY OF TUSCIA   (Italy)

more..

Author keywords

melanin; outlier test; passerine bird; SNP; ultraviolet reflectance

Indexed keywords

ADAPTATION; COLOR; DIVERGENCE; GENE; GENE EXPRESSION; GENETIC VARIATION; MELANIN; MOLECULAR ANALYSIS; NATURAL SELECTION; PASSERINE; PIGMENT; POPULATION STRUCTURE; REPRODUCTIVE BEHAVIOR; SIGNAL; ULTRAVIOLET RADIATION;

SPAIN;

AVES; FICEDULA HYPOLEUCA; PASSERIFORMES;

EID: 84858855254     PISSN: 0018067X     EISSN: 13652540     Source Type: Journal    
DOI: 10.1038/hdy.2011.93     Document Type: Article

References (72)

1. Andersson S, Prager M (2006). Quantifying Colors, Vol I-Mechanisms and Measurements. Harvard University Press: Cambridge. 589pp.
2. April CS, Jackson IJ, Kidson SH (1998). The cloning and sequencing of a cDNA coding for chick tyrosinase-related protein-1. Biochim Biophys Acta 1395: 7-12.
3. Beaumont MA, Balding DJ (2004). Identifying adaptive genetic divergence among populations from genome scans. Mol Ecol 13: 969-980.
4. Beaumont MA, Nichols RA (1996). Evaluating loci for use in the genetic analysis of population structure. Proc Natl Acad Sci USA 263: 1619-1626.
5. Bennett ATD, Cuthill IC, Partridge JC, Lunau K (1997). Ultraviolet plumage colors predict mate preferences in starlings. Proc Natl Acad Sci USA 94: 8618-8621.
6. Bennett DC, Lamoreux ML (2003). The color loci of mice-A genetic century. Pigment Cell Res 16: 333-344.
7. Bilezikjian LM, Corrigan AZ, Blount AL, Chen Y, Vale WW (2001). Regulation and actions of Smad7 in the modulation of activin, inhibin, and transforming growth factor-beta signaling in anterior pituitary cells. Endocrinology 142: 1065-1072.
8. Borge T, Webster MT, Andersson G, Saetre GP (2005). Contrasting patterns of polymorphism and divergence on the Z chromosome and autosomes in two Ficedula flycatcher species. Genetics 171: 1861-1873.
9. Boswell T, Takeuchi S (2005). Recent developments in our understanding of the avian melanocortin system: Its involvement in the regulation of pigmentation and energy homeostasis. Peptides 26: 1733-1743.
10. Boughman JW (2002). How sensory drive can promote speciation. Trends Ecol Evol 17: 571-577.
11. Buggiotti L (2007) Avian evolutionary genomics: Studies of Ficedula flycatchers. PhD thesis, University of Turku, Turku.
12. Clark DA, Coker R (1998). Transforming growth factor-beta (TGF-beta). Int J Biochem Cell Biol 30: 293-298.
13. Cuthill IC, Partridge JC, Bennett ATD, Church SC, Hart NS, Hunt S (2000). Ultraviolet Vision in Birds Advances in the Study of Behavior. Academic Press Inc.: San Diego. Vol. 29, pp 159-214.
14. Deng MX, Chen WL, Takatori A, Peng ZM, Zhang L, Mongan M et al. (2006). A role for the mitogen-activated protein kinase kinase kinase 1 in epithelial wound healing. Mol Biol Cell 17: 3446-3455.
15. Drost R (1936).Über das Brutkleid männlicher Trauerfliegenfänger, Muscicapa hypoleuca. Vogelzug 6: 179-186.
16. Endler JA, Westcott DA, Madden JR, Robson T (2005). Animal visual systems and the evolution of color patterns: Sensory processing illuminates signal evolution. Evolution 59: 1795-1818.
17. Excoffier L, Hofer T, Foll M (2009). Detecting loci under selection in a hierarchically structured population. Heredity 103: 285-298.
18. Excoffier L, Lischer HEL (2010). Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resources 10: 564-567.
19. Falcon-Perez JM, DellAngelica EC (2002). The pallidin (Pldn) gene and the role of SNARE proteins in melanosome biogenesis. Pigment Cell Res 15: 82-86.
20. Fitzpatrick MJ, Ben-Shahar Y, Smid HM, Vet LEM, Robinson GE, Sokolowski MB (2005). Candidate genes for behavioural ecology. Trends Ecol Evol 20: 96-104.
21. Fukuda M, Kuroda TS, Mikoshiba K (2002). Slac2-a/melanophilin, the missing link between Rab27 and myosin Va-implications of a tripartite protein complex for melanosome transport. J Biol Chem 277: 12432-12436.
22. Goudet J (1995). FSTAT (Version 1.2): A computer program to calculate F-statistics. J Hered 86: 485-486.
23. Glutz von Blotzheim UN, Bauer KM (1993). Handbuch der Vögel Mitteleuropas. Aula-Verlag, Wiesbaden.
24. Hall TA (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Series 41: 95-98.
25. Hubbard JK, Uy JAC, Hauber ME, Hoekstra HE, Safran RJ (2010). Vertebrate pigmentation: From underlying genes to adaptive function. Trends Genet 26: 231-239.
26. Hunt S, Cuthill IC, Bennett ATD, Griffiths R (1999). Preferences for ultraviolet partners in the blue tit. Animal Behav 58: 809-815.
27. Ito JI, Kuzumaki T, Otsu K, Iuchi Y, Ishikawa K (1998). Hormonal regulation of aldolase B gene expression in rat primary cultured hepatocytes. Arch Biochem Biophys 350: 291-297.
28. Jones KL, Mansell A, Patella S, Scott BJ, Hedger MP, de Kretser DM et al. (2007). Activin A is a critical component of the inflammatory response, and its binding protein, follistatin, reduces mortality in endotoxemia. Proc Natl Acad Sci USA 104: 16239-16244.
29. Kim DS, Rhew TH, Moss DJ, Kim JY (1999). cDNA cloning of the CEPUS, a secreted type of neural glycoprotein belonging to the immunoglobulin-like opioid binding cell adhesion molecule (OBCAM) subfamily. Mol Cells 9: 270-276.
30. Lamb TD (1986). Transduction in vertebrate photoreceptors: The roles of cyclic GMP and calcium. Trends Neurosci 9: 224-228.
31. Leal M, Fleishman LJ (2004). Differences in visual signal design and detectability between allopatric populations of Anolis lizards. Am Nat 163: 26-39.
32. Lehtonen PK (2010) The molecular mechanisms and evolutionary significance of plumage colour variation in pied flycatchers (Ficedula hypoleuca). PhD thesis, University of Turku, Turku.
33. Lehtonen PK, Laaksonen T, Artemyev AV, Belskii E, Both C, Bures S et al. (2009a). Geographic patterns of genetic differentiation and plumage colour variation are different in the pied flycatcher (Ficedula hypoleuca). Mol Ecol 18: 4463-4476.
34. Lehtonen PK, Primmer CR, Laaksonen T (2009b). Different traits affect gain of extrapair paternity and loss of paternity in the pied flycatcher, Ficedula hypoleuca. Animal Behav 77: 1103-1110.
35. Lundberg A, Alatalo RV (1992). The Pied Flycatcher. Poyser: London.
36. Maguire DJ, Day AR, Borthwick IA, Srivastava G, Wigley PL, May BK et al. (1986). Nucleotide sequence of the chicken-5-aminolevulinate synthase gene. Nucleic Acids Res 14: 1379-1391.
37. Mantel N (1967). Detection of disease clustering and a generalized regression approach. Cancer Res 27(2P1): 209-220.
38. Mullen P, Pohland G (2008). Studies on UV reflection in feathers of some 1000 bird species: Are UV peaks in feathers correlated with violet-sensitive and ultravioletsensitive cones? IBIS 150: 59-68.
39. Mundy NI (2005). A window on the genetics of evolution: MC1R and plumage colouration in birds. Proc R Soc B Biol Sci 272: 1633-1640.
40. Mundy NI, Kelly J, Theron E, Hawkins K (2003). Evolutionary genetics of the melanocortin-1 receptor in vertebrates. In: Cone RD (ed) Melanocortin System, Vol. 994, pp 307-312.
41. Nachman MW, Hoekstra HE, DAgostino SL (2003). The genetic basis of adaptive melanism in pocket mice. Proc Natl Acad Sci USA 100: 5268-5273.
42. Nadeau NJ, Mundy NI, Gourichon D, Minvielle F (2007). Association of a single-nucleotide substitution in TYRP1 with roux in Japanese quail (Coturnix japonica). Animal Genet 38: 609-613.
43. Noramly S, Morgan BA (1998). BMPs mediate lateral inhibition at successive stages in feather tract development. Development 125: 3775-3787.
44. Odeen A, Hart NS, Hastad O (2009). Assessing the use of genomic DNA as a predictor of the maximum absorbance wavelength of avian SWS1 opsin visual pigments. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 195: 167-173.
45. Ohyama A, Saito F, Ohuchi H, Noji S (2001). Differential expression of two BMP antagonists, gremlin and Follistatin, during development of the chick feather bud. Mech Dev 100: 331-333.
46. Okano T, Yoshizawa T, Fukada Y (1994). Pinopsin is a chicken pineal photoreceptive molecule. Nature 372: 94-97.
47. Patel K, Makarenkova H, Jung HS (1999). The role of long range, local and direct signalling molecules during chick feather bud development involving the BMPs, Follistatin and the Eph receptor tyrosine kinase Eph-A4. Mech Dev 86: 51-62.
48. Peakall R, Smouse PE (2006). GENALEX 6: Genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6: 288-295.
49. Primmer CR, Borge T, Lindell J, Saetre GP (2002). Single-nucleotide polymorphism characterization in species with limited available sequence information: High nucleotide diversity revealed in the avian genome. Mol Ecol 11: 603-612.
50. Raymond M, Rousset F (1995). GENEPOP (VERSION-1.2)-population-genetics software for exact tests and ecumenicism. J Hered 86: 248-249.
51. Rosenblum EB, Novembre J (2007). Ascertainment bias in spatially structured populations: A case study in the eastern fence lizard. J Hered 98: 331-336.
52. Rozen S, Skaletsky H (1999). Primer3 on the WWW for General Users and for Biologist Programmers, Vol. 132, pp 365-386.
53. Sabeti PC, Schaffner SF, Fry B, Lohmueller J, Varilly P, Shamovsky O et al. (2006). Positive natural selection in the human lineage. Science 312: 1614-1620.
54. Saetre GP, Saether SA (2010). Ecology and genetics of speciation in Ficedula flycatchers. Mol Ecol 19: 1091-1106.
55. Schoenborn V, Gohlke H, Heid IM, Illig T, Utermann G, Kronenberg F (2007). Sample selection algorithm to improve quality of genotyping from plasma-derived DNA: To separate the wheat from the chaff. Hum Mutat 28: 1141-1149.
56. Seehausen O, Terai Y, Magalhaes IS, Carleton KL, Mrosso HDJ, Miyagi R et al. (2008). Speciation through sensory drive in cichlid fish. Nature 455: 620-U623.
57. Siitari H, Honkavaara J, Huhta E, Viitala J (2002). Ultraviolet reflection and female mate choice in the pied flycatcher, Ficedula hypoleuca. Animal Behav 63: 97-102.
58. SirkiäPM (2011) Maintenance of phenotypic variation in plumage colouration in a passerine bird. PhD thesis, University of Turku, Turku.
59. Sirki äPM, Laaksonen T (2009). Distinguishing between male and territory quality: Females choose multiple traits in the pied flycatcher. Animal Behav 78: 1051-1060.
60. Stephens M, Donnelly P (2003). A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73: 1162-1169.
61. Takahashi S, Kawarabayasi Y, Nakai T, Sakai J, Yamamoto T (1992). Rabbit very low-density-lipoprotein receptor-A low-density-lipoprotein receptor-like protein with distinct ligand specificity. Proc Natl Acad Sci USA 89: 9252-9256.
62. Vasemagi A, Primmer CR (2005). Challenges for identifying functionally important genetic variation: The promise of combining complementary research strategies. Mol Ecol 14: 3623-3642.
63. Weber TP, Borgudd J, Hedenstrom A, Persson K, Sandberg G (2005). Resistance of flight feathers to mechanical fatigue covaries with moult strategy in two warbler species. Biol Lett 1: 27-30.
64. Wegner A (1979). Equilibrium of the actin-tropomyosin interaction. J Mol Biol 131: 839-853.
65. Widelitz RB, Jiang TX, Yu MK, Shen T, Shen JY, Wu P et al. (2003). Molecular biology of feather morphogenesis: A testable model for evo-devo research. J Exp Zool B Mol Dev Evol 298B: 109-122.
66. Widlund HR, Fisher DE (2003). Microphthalamia-associated transcription factor: A critical regulator of pigment cell development and survival. Oncogene 22: 3035-3041.
67. Wilkie SE, Robinson PR, Cronin TW, Poopalasundaram S, Bowmaker JK, Hunt DM (2000). Spectral tuning of avian violet-and ultraviolet-sensitive visual pigments. Biochemistry 39: 7895-7901.
68. Wood HM, Grahame JW, Humphray S, Rogers J, Butlin RK (2008). Sequence differentiation in regions identified by a genome scan for local adaptation. Mol Ecol 17: 3123-3135.
69. Wright S (1969) vol. 2, the Theory of Gene Frequencies University of Chicago Press: Chicago, IL.
70. Yamane K, Ihn H, Asano Y, Jinnin M, Tamaki K (2003). Antagonistic effects of TNF-alpha on TGF-beta signaling through downregulation of TGF-beta receptor type II in human dermal fibroblasts. J Immunol 171: 3855-3862.
71. Yokoyama S, Radlwimmer FB, Kawamura S (1998). Regeneration of ultraviolet pigments of vertebrates. FEBS Lett 423: 155-158.
72. Ödeen A, Hart NS, Hastad O (2009). Assessing the use of genomic DNA as a predictor of the maximum absorbance wavelength of avian SWS1 opsin visual pigments. J Comp Physiol 195: 167-173.