Polymorphism at the Clock gene predicts phenology of long-distance migration in birds

Molecular Ecology

Volumn 24, Issue 8, 2015, Pages 1758-1773

  Saino, Nicola ^a   Bazzi, Gaia ^a   Gatti, Emanuele ^a   Caprioli, Manuela ^a   Cecere, Jacopo G ^b   Possenti, Cristina D ^a   Galimberti, Andrea ^c   Orioli, Valerio ^c   Bani, Luciano ^c   Rubolini, Diego ^a   Gianfranceschi, Luca ^a   Spina, Fernando ^b  

^a UNIVERSITY OF MILAN   (Italy)

^b INSTITUTE FOR ENVIRONMENTAL PROTECTION AND RESEARCH ISPRA   (Italy)

^c UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

Adcyap1; Anthus trivialis; birds; climate change; Clock; Ficedula hypoleuca; Luscinia megarhynchos; migration; phenology; Saxicola rubetra

Indexed keywords

ANTHUS TRIVIALIS; AVES; FICEDULA HYPOLEUCA; LUSCINIA MEGARHYNCHOS; SAXICOLA RUBETRA;

HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; TRANSCRIPTION FACTOR CLOCK;

ALLELE; ANIMAL; CIRCADIAN RHYTHM; FEMALE; GENETIC POLYMORPHISM; GENETICS; MALE; PHENOTYPE; POPULATION MIGRATION; SONGBIRD; STATISTICAL MODEL;

ALLELES; ANIMAL MIGRATION; ANIMALS; CIRCADIAN RHYTHM; CLOCK PROTEINS; FEMALE; LINEAR MODELS; MALE; PASSERIFORMES; PHENOTYPE; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; POLYMORPHISM, GENETIC;

EID: 84933576336     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.13159     Document Type: Article

References (91)

1. Bairlein F, (1995) European-African Songbird Migration Network. Manual of field Methods. IFV, Wilhelmshaven, Germany.
2. Beacham TD, Murray CB, (1988) Influence of photoperiod and temperature on timing of sexual maturity of pink salmon (Oncorhynchus gorbucha). Canadian Journal of Zoology, 66, 1729-1732.
3. Bell-Pedersen D, Cassone VM, Earnest DJ, et al,. (2005) Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nature Reviews Genetics, 6, 544-556.
4. Berthold P, Gwinner E, Sonnenschein E, (2003) Avian Migration. Springer, Berlin.
5. Both C, Bouwhuis S, Lessells CM, et al,. (2006) Climate change and population declines in a long-distance migratory bird. Nature, 441, 81-83.
6. Both C, van Asch M, Bijlsma LG, et al,. (2009) Climate change and unequal phenological changes across four trophic levels: constraints or adaptations? Journal of Animal Ecology, 78, 73-83.
7. Bradshaw WE, Holzapfel CM, (2007) Evolution of animal photoperiodism. Annual Review of Ecology, Evolution, and Systematics, 38, 1-25.
8. Bradshaw WE, Holzapfel CM, (2010) Light, time, and the physiology of biotic response to rapid climate change in animals. Annual Review of Physiology, 72, 149-166.
9. Burns JR, (1985) The effect of low-latitude photoperiods on the reproduction of female and male Poeciliopsis gracilis and Poecilia sphenops. Copeia, 4, 961-965.
10. Caprioli M, Ambrosini R, Boncoraglio G, et al,. (2012) Clock gene variation is associated with breeding phenology and maybe under directional selection in the migratory barn swallow (Hirundo rustica). PLoS One, 7, e35140.
11. Chakarov N, Jonker RM, Boerner M, et al,. (2013) Variation at candidate genes correlates with timing of dispersal and plumage morph in a sedentary bird of prey. Molecular Ecology, 22, 5430-5440.
12. Clutton-Brock TH, (1988) Reproductive Success. University of Chicago Press, Chicago.
13. Cramp S, (1998) The Complete Birds of the Western Palearctic on CD-ROM. Oxford University Press, Oxford.
14. Dawson A, (2004) The effects of delaying the start of moult on the duration of moult, primary feather growth rates and feather mass in Common Starlings Sturnus vulgaris. Ibis, 3, 493-500.
15. Dawson A, King VM, Bentley GE, et al,. (2001) Photoperiodic control of seasonality in birds. Journal of Biological Rhythms, 16, 365-380.
16. Dejda A, Sokolowska P, Nowak JZ, (2005) Neuroprotective potential of three neuropeptides PACAP, VIP and PHI. Pharmacological Reports, 57, 307-320.
17. Dor R, Lovette IJ, Safran RJ, et al,. (2011) Low variation in the polymorphic Clock Poly-Q region despite population genetic structure across Barn Swallow (Hirundo rustica) populations. PLoS One, 6, e28843.
18. Dor R, Cooper CB, Lovette IJ, et al,. (2012) Clock gene variation in Tachycineta swallows. Ecology and Evolution, 2, 95-105.
19. Dunn PO, Winkler DW, (2010) Effects of climate change on timing of breeding and reproductive success in birds. In: Effects of Climate Change on Birds (eds, Møller AP, Fiedler W, Berthold P,), pp. 129-147. Oxford University Press, Oxford.
20. Ellegren H, Sheldon BC, (2008) Genetic basis for fitness differences in natural populations. Nature, 452, 169-175.
21. Evans K, Gaston KJ, Sharp SP, et al,. (2009) The effect of urbanisation on avian morphology and latitudinal gradients in body size. Oikos, 118, 251-259.
22. Fidler AE, Gwinner E, (2003) Comparative analysis of avian BMAL1 and CLOCK protein sequences: a search for features associated with owl nocturnal behaviour. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 136, 861-874.
23. Foster RG, Kreitzman L, (2009) Seasons of Life: the Biological Rhythms That Enable Living Things to Thrive and Survive. Yale University Press, New Haven, Connecticut.
24. Gekakis N, Staknis D, Nguyen HB, et al,. (1998) Role of the CLOCK protein in the mammalian circadian mechanism. Science, 280, 1564-1569.
25. Goymann W, Spina F, Ferri A, Fusani L, (2010) Body fat influences departure from stopover sites in migratory birds: evidence from whole-island telemetry. Biology Letters, 6, 478-481.
26. Gwinner E, (1986) Circadian rhythms in the control of avian migration. Advances in the Study of Behavior, 16, 191-228.
27. Gwinner E, (1996) Circadian and circannual programmes in avian migration. The Journal of Experimental Biology, 199, 39-48.
28. Gwinner E, (2003) Circannual rhythms in birds. Current Opinion in Neurobiology, 13, 770-778.
29. Hands S, Sinadinos C, Wyttenbach A, (2008) Polyglutamine gene function and dysfunction in the ageing brain. Biochimica et Biophysica Acta-Gene Regulatory Mechanisms, 1779, 507-521.
30. Hau M, Wikelski M, Wingfield JC, (1998) A Neotropical forest bird can measure the slight changes in tropical photoperiod. Proceedings of the Royal Society B, 265, 89-95.
31. Hayasaka N, LaRue SI, Green CB, (2002) In vivo disruption of Xenopus CLOCK in the retinal photoreceptor cells abolishes circadian melatonin rhythmicity without affecting its production levels. Journal of Neuroscience, 22, 1600-1607.
32. Helm B, (2009) Temporal coordination of life cycle stages: an avian chronobiology perspective. Integrative and Comparative Biology, 49, E73.
33. Helm B, Ben-Shlomo R, Sheriff MJ, et al,. (2013) Annual rhythms that underlie phenology: biological time-keeping meets environmental change. Proceedings of the Royal Society B: Biological Sciences, 280, 1-10.
34. Jenni L, Winkler R, (1994) Moult and Ageing of European Passerines. Academic Press, London.
35. Jenni L, Jenni-Eiermann S, Spina F, et al,. (2000) Regulation of protein breakdown and adrenocortical response to stress in birds during migratory flight. American Journal of Physiology, 278, R1182-R1189.
36. Johnsen A, Fiedler AE, Kuhn S, et al,. (2007) Avian Clock gene polymorphism: evidence for a latitudinal cline in allele frequencies. Molecular Ecology, 16, 4867-4880.
37. Jonzén N, Piacentini D, Andersson A, et al,. (2006) The timing of spring migration in trans-Saharan migrants: a comparison between Ottenby, Sweden and Capri, Italy. Ornis Svecica, 16, 27-33.
38. Kaiser A, (1993) A new multi-category classification of subcutaneous fat deposits of songbirds. Journal of Field Ornithology, 64, 246-255.
39. Knudsen E, Linden A, Both C, et al,. (2011) Challenging claims in the study of migratory birds and climate change. Biological Reviews, 86, 928-946.
40. Ko CH, Takahashi JS, (2006) Molecular components of the mammalian circadian clock. Human Molecular Genetics, 15, 271-277.
41. Kuhn K, Schwenk K, Both C, et al,. (2013) Differentiation in neutral genes and a candidate gene in the pied flycatcher: using biological archives to track global climate change. Ecology and Evolution, 3, 4799-4814.
42. Lee JCI, Tsai L-C, Hwa P-Y, et al,. (2010) A novel strategy for avian species and gender identification using the CHD gene. Molecular and Cellular Probes, 24, 27-31.
43. Lehikoinen E, Sparks TH, (2010) Changes in migration. In: Effects of Climate Change on Birds (eds, Møller AP, Fiedler W, Berthold P,), pp. 89-112. Oxford University Press, Oxford.
44. Li YC, Korol AB, Fahima T, Nevo E, (2004) Microsatellites within genes: structure, function, and evolution. Molecular Biology and Evolution, 21, 991-1007.
45. Liechti F, Scandolara C, Rubolini D, et al,. (2015) Timing of migration and residence areas during the non-breeding period of barn swallows Hirundo rustica in relation to sex and population. Journal of Avian Biology, 45, 1-12.
46. Liedvogel M, Sheldon BC, (2010) Low variability and absence of phenotypic correlates of Clock gene variation in a great tit Parus major population. Journal of Avian Biology, 41, 543-550.
47. Liedvogel M, Szulkin M, Knowles SCL, et al,. (2009) Phenotypic correlates of Clock gene variation in a wild blue tit population: evidence for a role in seasonal timing of reproduction. Molecular Ecology, 18, 2444-2456.
48. Meschini E, Frugis S, (1993) Atlante degli uccelli nidificanti in Italia. Istituto Nazionale di Biologia della Selvaggina, Ozzano Emilia.
49. Mirabella N, Squillacioti C, Colitti M, et al,. (2002) Pituitary adenylate cyclase activating peptide (PACAP) immunoreactivity and mRNA expression in the duck gastrointestinal tract. Cell and Tissue Research, 308, 347-359.
50. Møller AP, Rubolini D, Lehikoinen E, (2008) Populations of migratory bird species that did not show a phenological response to climate change are declining. Proceedings of the National Academy of Sciences, 105, 16195-16200.
51. Møller AP, Fiedler W, Berthold P, (eds) (2010) Effects of Climate Change on Birds. Oxford University Press, Oxford.
52. Mueller J, Pulido F, Kempenaers B, (2011) Identification of a gene associated with avian migratory behaviour. Proceedings of the Royal Society B, 278, 2848-2856.
53. Nagy AD, Csernus VJ, (2007) The role of PACAP in the control of circadian expression of clock genes in the chicken pineal gland. Peptides, 28, 1767-1774.
54. Nussey DH, Postma E, Gienapp P, et al,. (2005) Selection on heritable phenotypic plasticity in a wild bird population. Science, 310, 304-306.
55. O'Brien C, Unruh L, Zimmerman C, et al,. (2013) Geography of the circadian gene clock and photoperiodic response in western North American populations of the three-spined stickleback Gasterosteus aculeatus. Journal of Fish Biology, 82, 827-839.
56. O'Malley KG, Banks MA, (2008) A latitudinal cline in the Chinook salmon (Oncorhynchus tshawytscha) Clock gene: evidence for selection on PolyQ length variants. Proceedings of the Royal Society B, 275, 2813-2821.
57. O'Malley KG, Ford MJ, Hard JJ, (2010) Clock polymorphism in Pacific salmon: evidence for variable selection along a latitudinal gradient. Proceedings of the Royal Society B, 227, 3703-3714.
58. Panda S, Hogenesch JB, Kay SA, (2002) Circadian rhythms from flies to human. Nature, 417, 329-335.
59. Peirõ G, (2003) Intraspecific variation in the wing shape of the long-distance migrant reed warbler Acrocephalus scirpaceus: effects of age and distance of migration. Ardeola, 50, 31-37.
60. Peterson MP, Abolins-Abols M, Atwell JW, et al,. (2013) Variation in candidate genes CLOCK and ADCYAP1 does not consistently predict differences in migratory behavior in the songbird genus Junco. F1000Research, 2, 115.
61. Pulido F, (2007) The genetics and evolution of avian migration. BioScience, 57, 165-174.
62. Pulido F, Widmer M, (2005) Are long-distance migrants constrained in their evolutionary response to environmental change? Causes of variation in the timing of autumn migration in a blackcap (S. atricapilla) and two garden warbler (Sylvia borin) populations. Annals of the New York Academy of Sciences, 1046, 228-241.
63. Racz B, Horvath G, Faluhelyi N, et al,. (2008) Effects of PACAP on the circadian changes of signaling pathways in chicken pinealocytes. Journal of Molecular Neuroscience, 36, 220-226.
64. Riley DE, Krieger JN, (2009) UTR dinucleotide simple sequence repeat evolution exhibits recurring patterns including regulatory sequence motif replacements. Gene, 429, 80-86.
65. Riley BE, Orr HT, (2006) Polyglutamine neurodegenerative diseases and regulation of transcription: assembling the puzzle. Genes & Development, 20, 2183-2192.
66. Ross CA, (2002) Polyglutamine pathogenesis: emergence of unifying mechanisms for Huntington's disease and related disorders. Neuron, 35, 819-822.
67. Rubolini D, Spina F, Saino N, (2005) Correlates of timing of spring migration in birds: a comparative study of trans-Saharan migrants. Biological Journal of the Linnean Society, 85, 199-210.
68. Rubolini D, Møller AP, Rainio K, et al,. (2007) Intraspecific consistency and geographic variability in temporal trends of spring migration phenology among European bird species. Climate Research, 35, 135-146.
69. Rubolini D, Møller AP, Saino N, (2010) Migratory behaviour constrains the phenological response of birds to climate change. Climate Research, 42, 45-55.
70. Saino N, Ambrosini R, (2008) Climatic connectivity between Africa and Europe may serve as a basis for phenotypic adjustment of migration schedules of trans-Saharan migratory birds. Global Change Biology, 14, 250-263.
71. Saino N, Martinelli R, Romano M, (2008) Ecological and phenological covariates of offspring sex ratio in barn swallows. Evolutionary Ecology, 22, 659-674.
72. Saino N, Rubolini D, Serra L, et al,. (2010a) Sex-related variation in migration phenology in relation to sexual dimorphism: a test of competing hypotheses for the evolution of protandry. Journal of Evolutionary Biology, 23, 2054-2065.
73. Saino N, Rubolini D, von Hardenberg J, et al,. (2010b) Spring migration decisions in relation to weather are predicted by wing morphology among trans-Mediterranean migratory birds. Functional Ecology, 24, 658-669.
74. Saino N, Ambrosini R, Rubolini D, et al,. (2011) Climate warming, ecological mismatch at arrival and population decline in migratory birds. Proceedings of the Royal Society B, 278, 835-842.
75. Saino N, Romano M, Caprioli M, et al,. (2013) Timing of molt of barn swallows is delayed in a rare Clock genotype. PeerJ, 1, e17.
76. Saleem Q, Anand A, Jain S, et al,. (2001) The polyglutamine motif is highly conserved at the Clock locus in various organisms and is not polymorphic in humans. Human Genetics, 109, 136-142.
77. Sanderson FJ, Donald PF, Pain DJ, et al,. (2006) Long-term population declines in Afro-Palearctic migrant birds. Biological Conservation, 131, 93-105.
78. Schwartz MD, Ahas R, Aasa A, (2006) Onset of spring starting earlier across the Northern Hemisphere. Global Change Biology, 12, 343-351.
79. Sharp PJ, (2005) Photoperiodic regulation of seasonal breeding in birds. Annals of the New York Academy of Sciences, 1040, 189-199.
80. Spina F, Volponi S, (2008) Atlante della Migrazione degli Uccelli in Italia. Vol. 2: Passeriformi, pp. 629. ISPRA-MATTM, Roma.
81. Spina F, Massi A, Montemaggiori A, et al,. (1993) Spring migration across Central Mediterranean: general results from the 'Progetto Piccole Isole'. Vogelwarte, 37, 1-94.
82. Steinmeyer C, Mueller JC, Kempenaers B, (2009) Search for informative polymorphism in candidate genes: clock genes and circadian behaviour in blue tits. Genetica, 136, 109-117.
83. Svensson L, (1992) Identification Guide to European Passerines. Privately published, Stockholm.
84. Tarka M, Åkesson M, Beraldi D, et al,. (2010) A strong quantitative trait locus for wing length on chromosome 2 in a wild population of great reed warblers. Proceedings of the Royal Society B, 277, 2361-2369.
85. Tauber E, Kyriacou CP, (2005) Molecular evolution and population genetics of circadian clock genes. Methods in Enzymology, 393, 797-817.
86. Tenan S, Spina F, (2010) Timing and condition-related effects on recapture probability, mass change and stopover length of spring migrating songbirds on a small Mediterranean island. Ardeola, 57, 121-132.
87. Vágási CI, Pap PL, Barta Z, (2010) Haste makes waste: accelerated molt adversely affects the expression of melanin-based and depigmented plumage ornaments in house sparrows. PLoS One, 5, e14215.
88. Vaudry D, Falluel-Morel A, Bourgault S, et al,. (2009) Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacological Reviews, 6, 283-357.
89. Vaz Nunes M, Saunders D, (1999) Photoperiodic time measurement in insects: a review of clock models. Journal of Biological Rhythms, 14, 84-104.
90. Visser ME, Caro SP, van Oers K, et al,. (2010) Phenology, seasonal timing and circannual rhythms: towards a unified frame work. Philosophical Transactions of the Royal Society B: Biological Sciences, 365, 3113-3127.
91. Wayne NL, Rissman EF, (1991) Tropical photoperiods affect reproductive development in the musk shrew, Suncus murinus. Physiology & Behavior, 50, 549-553.