Seasonal timing and population divergence: When to breed, when to migrate

Current Opinion in Behavioral Sciences

Volumn 6, Issue , 2015, Pages 50-58

  Ketterson, Ellen D ^a   Fudickar, Adam M ^a   Atwell, Jonathan W ^a   Greives, Timothy J ^b  

^a INDIANA UNIVERSITY   (United States)

^b NORTH DAKOTA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIODIVERSITY; BREEDING; CLIMATE; ENVIRONMENTAL FACTOR; NONHUMAN; POPULATION MIGRATION; REPRODUCTION; REVIEW; SEASONAL POPULATION DYNAMICS; SEASONAL VARIATION; TIME PERCEPTION;

EID: 84942256574     PISSN: None     EISSN: 23521546     Source Type: Journal    
DOI: 10.1016/j.cobeha.2015.09.001     Document Type: Review

References (98)

1. Visser M.E., Caro S.P., van Oers K., Schaper S.V., Helm B. Phenology, seasonal timing and circannual rhythms: towards a unified framework. Philos Trans R Soc Lond B: Biol Sci 2010, 365:3113-3127.
2. Charmantier A., McCleery R.H., Cole L.R., Perrins C., Kruuk L.E., Sheldon B.C. Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 2008, 320:800-803.
3. Gienapp P., Lof M., Reed T.E., McNamara J., Verhulst S., Visser M.E. Predicting demographically sustainable rates of adaptation: can great tit breeding time keep pace with climate change?. Philos Trans R Soc B: Biol Sci 2013, 368:20120289.
4. Pulido F., Berthold P. Current selection for lower migratory activity will drive the evolution of residency in a migratory bird population. PNAS 2010, 107:7341-7346.
5. Rubolini D., Møller A.P., Rainio K., Lehikoinen E. Intraspecific consistency and geographic variability in temporal trends of spring migration phenology among European bird species. Clim Res 2007, 35:135-146.
6. Gill J.A., Alves J.A., Sutherland W.J., Appleton G.F., Potts P.M., Gunnarsson T.G. Why is timing of bird migration advancing when individuals are not?. Proc R Soc B: Biol Sci 2014, 281:20132161.
7. Heath J.A., Steenhof K., Foster M.A. Shorter migration distances associated with higher winter temperatures suggest a mechanism for advancing nesting phenology of American kestrels Falco sparverius. J Avian Biol 2012, 43:376-384.
8. Devaux C., Lande R. Incipient allochronic speciation due to non-selective assortative mating by flowering time, mutation and genetic drift. Proc R Soc B: Biol Sci 2008, 275:2723-2732.
9. Adams R.A., Thibault K.M. Temporal resource partitioning by bats at water holes. J Zool 2006, 270:466-472.
10. Quinn T.P., Unwin M.J., Kinnison M.T. Evolution of temporal isolation in the wild: genetic divergence in timing of migration and breeding by introduced chinook salmon populations. Evolution 2000, 54:1372-1385.
11. Dor R., Safran R.J., Vortman Y., Lotem A., McGowan A., Evans M.R., Lovette I.J. Population genetics and morphological comparisons of migratory European (Hirundo rustica rustica) and sedentary east-Mediterranean (Hirundo rustica transitiva) Barn Swallows. J Hered 2012, 103:55-63.
12. Friesen V.L., Smith A.L., Gómez-Díaz E., Bolton M., Furness R.W., González-Solís J., Monteiro L.R. Sympatric speciation by allochrony in a seabird. PNAS 2007, 104:18589-18594.
13. Wingfield J.C. Regulatory mechanisms that underlie phenology, behavior, and coping with environmental perturbations: an alternative look at biodiversity. Auk 2012, 129:1-7.
14. Evans J.A., Leise T.L., Castanon-Cervantes O., Davidson A.J. Neural correlates of individual differences in circadian behaviour. Proc Biol Sci 2015, 282:20150769.
15. Watts H.E., MacDougall-Shackleton S.A., Hahn T.P. Variation among individuals in photoperiod responses: effects of breeding schedule, photoperiod, and age-related photoperiodic experience in birds. J Exp Zool A: Ecol Genet Physiol 2015, 323:368-374.
16. Helm B., Visser M.E. Heritable circadian period length in a wild bird population. Proc R Soc B: Biol Sci 2010, 277:3335-3342.
17. Winker K. On the origin of species through heteropatric differentiation: a review and a model of speciation in migratory animals. Ornithological Monographs 2010, vol 69:1-30. American Ornithologists' Union.
18. Kleindorfer S., O'Connor J.A., Dudaniec R.Y., Myers S.A., Robertson J., Sulloway F.J. Species collapse via hybridization in Darwin's tree finches. Am Nat 2014, 183:325-341.
19. Ball G.F., Balthazart J. Seasonal changes in the neuroendocrine system: introduction to the special issue. Front Neuroendocrinol 2015, 37:1-2.
20. Kriegsfeld L.J., Ubuka T., Bentley G.E., Tsutsui K. Seasonal control of gonadotropin-inhibitory hormone (GnIH) in birds and mammals. Front Neuroendocrinol 2015, 37:65-75.
21. Wingfield J.C. Coping with change: a framework for environmental signals and how neuroendocrine pathways might respond. Front Neuroendocrinol 2015, 37:89-96.
22. Singh J., Budki P., Rani S., Kumar V. Temperature alters the photoperiodically controlled phenologies linked with migration and reproduction in a night-migratory songbird. Proc Biol Sci 2012, 279:509-515.
23. Stenseth N.C., Durant J.M., Fowler M.S., Matthysen E., Adriaensen F., Jonzén N., Chan K.-S., Liu H., De Laet J., Sheldon B.C., et al. Testing for effects of climate change on competitive relationships and coexistence between two bird species. Proc R Soc B 2015, 282.
24. Dawson A. Annual gonadal cycles in birds: modeling the effects of photoperiod on seasonal changes in GnRH-1 secretion. Front Neuroendocrinol 2015, 37:52-64.
25. Grace J.K., Anderson D.J. Corticosterone stress response shows long-term repeatability and links to personality in free-living Nazca boobies. Gen Comp Endocrinol 2014, 208:39-48.
26. Baugh A.T., van Oers K., Naguib M., Hau M. Initial reactivity and magnitude of the acute stress response associated with personality in wild great tits (Parus major). Gen Comp Endocrinol 2013, 189:96-104.
27. Wingfield J., Sapolsky R. Reproduction and resistance to stress: when and how. J Neuroendocrinol 2003, 15:711-724.
28. Cockrem J.F. Corticosterone responses and personality in birds: individual variation and the ability to cope with environmental changes due to climate change. Gen Comp Endocrinol 2013, 190:156-163.
29. Jenkins B.R., Vitousek M.N., Hubbard J.K., Safran R.J. An experimental analysis of the heritability of variation in glucocorticoid concentrations in a wild avian population. Proc R Soc B: Biol Sci 2014, 281.
30. Banerjee S.B., Arterbery A.S., Fergus D.J., Adkins-Regan E. Deprivation of maternal care has long-lasting consequences for the hypothalamic-pituitary-adrenal axis of zebra finches. Proc R Soc B: Biol Sci 2012, 279:759-766.
31. Romero L.M. Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen Comp Endocrinol 2002, 128:1-24.
32. Lattin C.R., Romero L.M. Seasonal variation in corticosterone receptor binding in brain, hippocampus, and gonads in House Sparrows (Passer domesticus). Auk 2013, 130:591-598.
33. Son Y.L., Ubuka T., Narihiro M., Fukuda Y., Hasunuma I., Yamamoto K., Belsham D.D., Tsutsui K. Molecular basis for the activation of gonadotropin-inhibitory hormone gene transcription by corticosterone. Endocrinology 2014, 155:1817-1826.
34. Tobari Y., Son Y.L., Ubuka T., Hasegawa Y., Tsutsui K. A new pathway mediating social effects on the endocrine system: female presence acting via norepinephrine release stimulates gonadotropin-inhibitory hormone in the paraventricular nucleus and suppresses luteinizing hormone in quail. J Neurosci 2014, 34:9803-9811.
35. Ernst D., Lynn S., Bentley G. Differential response of GnIH in brain and gonads following acute stress in a songbird. Gen Comp Endocrinol 2015.
36. McGuire N.L., Koh A., Bentley G.E. The direct response of the gonads to cues of stress in a temperate songbird species is season-dependent. PeerJ 2013, 1:e139.
37. Wang G., Ramenofsky M., Wingfield J.C. Apparent dissociation of photoperiodic time measurement between vernal migration and breeding under dim green light conditions in Gambel's white-crowned sparrow Zonotrichia leucophrys gambelii. Curr Zool 2013, 59:349-359.
38. Bridge E.S., Thorup K., Bowlin M.S., Chilson P.B., Diehl R.H., Fléron R.W., Hartl P., Kays R., Kelly J.F., Robinson W.D., et al. Technology on the move: recent and forthcoming innovations for tracking migratory birds. Bioscience 2011, 61:689-698.
39. Chabot A.A., Hobson K.A., Van Wilgenburg S.L., McQuat G.J., Lougheed S.C. Advances in linking wintering migrant birds to their breeding-ground origins using combined analyses of genetic and stable isotope markers. PLoS ONE 2012, 7:e43627.
40. Rundel C.W., Wunder M.B., Alvarado A.H., Ruegg K.C., Harrigan R., Schuh A., Kelly J.F., Siegel R.B., DeSante D.F., Smith T.B., et al. Novel statistical methods for integrating genetic and stable isotope data to infer individual-level migratory connectivity. Mol Ecol 2013, 22:4163-4176.
41. Rushing C.S., Ryder T.B., Saracco J.F., Marra P.P. Assessing migratory connectivity for a long-distance migratory bird using multiple intrinsic markers. Ecol Appl 2014, 24:445-456.
42. Bowen G.J., Liu Z., Vander Zanden H.B., Zhao L., Takahashi G. Geographic assignment with stable isotopes in IsoMAP. Methods Ecol Evol 2014, 5:201-206.
43. Ruegg K.C., Anderson E.C., Paxton K.L., Apkenas V., Lao S., Siegel R.B., DeSante D.F., Moore F., Smith T.B. Mapping migration in a songbird using high-resolution genetic markers. Mol Ecol 2014, 23:5726-5739.
44. Bonter D.N., Cooper C.B. Data validation in citizen science: a case study from Project FeederWatch. Front Ecol Environ 2012, 10:305-307.
45. Princé K., Zuckerberg B. Climate change in our backyards: the reshuffling of North America's winter bird communities. Global Change Biol 2015, 21:572-585.
46. Boyle W.A., Norris D.R., Guglielmo C.G. Storms drive altitudinal migration in a tropical bird. Proc Biol Sci 2010, 277:2511-2519.
47. Fudickar A.M., Schmidt A., Hau M., Quetting M., Partecke J. Female-biased obligate strategies in a partially migratory population. J Anim Ecol 2013, 82:863-871.
48. Tonra C.M., Marra P.P., Holberton R.L. Experimental and observational studies of seasonal interactions between overlapping life history stages in a migratory bird. Horm Behav 2013, 64:825-832.
49. Owen J., Garvin M., Moore F. Elevated testosterone advances onset of migratory restlessness in a nearctic-neotropical landbird. Behav Ecol Sociobiol 2014, 68:561-569.
50. Ramenofsky M., Németh Z. Regulatory mechanisms for the development of the migratory phenotype: roles for photoperiod and the gonad. Horm Behav 2014, 66:148-158.
51. Nilsson A.L., Sandell M.I. Stress hormone dynamics: an adaptation to migration?. Biol Lett 2009, 5:480-483.
52. Eikenaar C., Klinner T., Stöwe M. Corticosterone predicts nocturnal restlessness in a long-distance migrant. Horm Behav 2014, 66:324-329.
53. Wagner D.N., Green D.J., Cooper J.M., Love O.P., Williams T.D. Variation in plasma corticosterone in migratory songbirds: a test of the migration-modulation hypothesis. Physiol Biochem Zool 2014, 87:695-703.
54. Landys M.M., Ramenofsky M., Guglielmo C.G., Wingfield J.C. The low-affinity glucocorticoid receptor regulates feeding and lipid breakdown in the migratory Gambel's white-crowned sparrow Zonotrichia leucophrys gambelii. J Exp Biol 2004, 207:143-154.
55. Holberton R., Morgan Wilson L., Hunter R., Cash W., Sims C. The role of corticosterone in supporting migratory lipogenesis in the dark-eyed junco, Junco hyemalis: a model for central and peripheral regulation. Physiol Biochem Zool 2007, 80:125-137.
56. Fusani L., Gwinner E. Simulation of migratory flight and stopover affects night levels of melatonin in a nocturnal migrant. Proc R Soc Lond B: Biol Sci 2004, 271:205-211.
57. Fusani L., Gwinner E. Melatonin and nocturnal migration. Ann NY Acad Sci 2005, 1046:264-270.
58. Fusani L., Cardinale M., Schwabl I., Goymann W. Food availability but not melatonin affects nocturnal restlessness in a wild migrating passerine. Horm Behav 2011, 59:187-192.
59. Jacobs J.D., Wingfield J.C. Endocrine control of life-cycle stages: a constraint on response to the environment?. Condor 2000, 102:35-51.
60. Tonra C.M., Marra P.P., Holberton R.L. Migration phenology and winter habitat quality are related to circulating androgen in a long-distance migratory bird. J Avian Biol 2011, 42:397-404.
61. Visser M.E., Gienapp P., Husby A., Morrisey M., de la Hera I., Pulido F., Both C. Effects of spring temperatures on the strength of selection on timing of reproduction in a long-distance migratory gird. PLoS Biol 2015, 13:e1002120.
62. Kristensen N.P., Johansson J., Ripa J., Jonzén N. Phenology of two interdependent traits in migratory birds in response to climate change. Proc R Soc B 2015, 282.
63. Perfito N., Jeong S.Y., Silverin B., Calisi R.M., Bentley G.E., Hau M. Anticipating spring: wild populations of great tits (Parus major) differ in expression of key genes for photoperiodic time measurement. PLoS ONE 2012, 7:e34997.
64. Liedvogel M., Sheldon B.C. Low variability and absence of phenotypic correlates of Clock gene variation in a great tit Parus major population. J Avian Biol 2010, 41:543-550.
65. Ouyang J.Q., Sharp P., Quetting M., Hau M. Endocrine phenotype, reproductive success and survival in the great tit, Parus major. J Evol Biol 2013, 26:1988-1998.
66. Da Silva A., Valcu M., Kempenaers B. Light pollution alters the phenology of dawn and dusk singing in common European songbirds. Philos Trans R Soc Lond B: Biol Sci 2015, 370.
67. Liedvogel M., Cornwallis C.K., Sheldon B.C. Integrating candidate gene and quantitative genetic approaches to understand variation in timing of breeding in wild tit populations. J Evol Biol 2012, 25:813-823.
68. Liedvogel M., Szulkin M., Knowles S.C.L., Wood M.J., Sheldon B.C. Phenotypic correlates of Clock gene variation in a wild blue tit population: evidence for a role in seasonal timing of reproduction. Mol Ecol 2009, 18:2444-2456.
69. Johnsen A., Fidler A.E., Kuhn S., Carter K.L., Hoffmann A., Barr I.R., Biard C., Charmantier A., Eens M., Korsten P., et al. Avian Clock gene polymorphism: evidence for a latitudinal cline in allele frequencies. Mol Ecol 2007, 16:4867-4880.
70. Porlier M., Charmantier A., Bourgault P., Perret P., Blondel J., Garant D. Variation in phenotypic plasticity and selection patterns in blue tit breeding time: between- and within-population comparisons. J Anim Ecol 2012, 81:1041-1051.
71. Partecke J., Gwinner E. Increased sedentariness in European Blackbirds following urbanization: a consequence of local adaptation?. Ecology 2007, 88:882-890.
72. Partecke J., Gwinner E., Bensch S. Is urbanisation of European blackbirds (Turdus merula) associated with genetic differentiation?. J Ornithol 2006, 147:549-552.
73. Partecke J., Schwabl I., Gwinner E. Stress and the city: urbanization and its effects on the stress physiology in European Blackbirds. Ecology 2006, 87:1945-1952.
74. Partecke J., Van't Hof T.J., Gwinner E. Underlying physiological control of reproduction in urban and forest-dwelling European blackbirds Turdus merula. J Avian Biol 2005, 36:295-305.
75. Evans K.L., Newton J., Gaston K.J., Sharp S.P., McGowan A., Hatchwell B.J. Colonisation of urban environments is associated with reduced migratory behaviour, facilitating divergence from ancestral populations. Oikos 2012, 121:634-640.
76. Mueller J.C., Partecke J., Hatchwell B.J., Gaston K.J., Evans K.L. Candidate gene polymorphisms for behavioural adaptations during urbanization in blackbirds. Mol Ecol 2013, 22:3629-3637.
77. Mueller J.C., Pulido F., Kempenaers B. Identification of a gene associated with avian migratory behaviour. Proc R Soc B: Biol Sci 2011, 278:2848-2856.
78. Morganti M., Åkesson S., Pulido F. Decoupling of behavioural and morphological differentiation in a partially migratory bird population. Bird Study 2014, 62:29-38.
79. Rolshausen G., Hobson K., Schaefer H.M. Spring arrival along a migratory divide of sympatric blackcaps (Sylvia atricapilla). Oecologia 2010, 162:175-183.
80. Mettler R., Schaefer H.M., Chernetsov N., Fiedler W., Hobson K.A., Ilieva M., Imhof E., Johnsen A., Renner S.C., Rolshausen G., et al. Contrasting patterns of genetic differentiation among blackcaps (Sylvia atricapilla) with divergent migratory orientations in Europe. PLOS ONE 2013, 8:e81365.
81. Caprioli M., Ambrosini R., Boncoraglio G., Gatti E., Romano A., Romano M., Rubolini D., Gianfranceschi L., Saino N. Clock gene variation is associated with breeding phenology and maybe under directional selection in the migratory barn swallow. PLoS ONE 2012, 7:e35140.
82. Saino N., Romano M., Caprioli M., Fasola M., Lardelli R., Micheloni P., Scandolara C., Rubolini D., Gianfranceschi L. Timing of molt of barn swallows is delayed in a rare Clock genotype. PeerJ 2013, 1:e17.
83. Ambrosini R., Rubolini D., Moller A.P., Bani L., Clark J., Karcza Z., Vangeluwe D., du Feu C., Spina F., Saino N. Climate change and the long-term northward shift in the African wintering range of the barn swallow Hirundo rustica. Clim Res 2011, 49:131-141.
84. Atwell J.W., Cardoso G.C., Whittaker D.J., Campbell-Nelson S., Robertson K.W., Ketterson E.D. Boldness behavior and stress physiology in a novel urban environment suggest rapid correlated evolutionary adaptation. Behav Ecol 2012, 23:960-969.
85. Atwell J.W., Cardoso G.C., Whittaker D.J., Price T.D., Ketterson E.D. Hormonal, behavioral, and life-history traits exhibit correlated shifts in relation to population establishment in a novel environment. Am Nat 2014, 184:E147-E160.
86. Peterson M., Abolins-Abols M., Atwell J., Rice R., Mil· B., Ketterson E. Variation in candidate genes CLOCK and ADCYAP1 does not consistently predict differences in migratory behavior in the songbird genus Junco [v1; ref status: indexed]. F1000Research 2013, 2.
87. Fudickar A, Atwell J, Greives T, Ketterson E: Reproductive allochrony in seasonally sympatric populations maintained by differential response to photoperiod: implications for population divergence and response to climate change. 2015. (in review).
88. Perfito N., Tramontin A., Meddle S., Sharp P., Afik D., Gee J., Ishii S., Kikuchi M., Wingfield J. Reproductive development according to elevation in a seasonally breeding male songbird. Oecologia 2004, 140:201-210.
89. Addis E., Davis J., Miner B., Wingfield J. Variation in circulating corticosterone levels is associated with altitudinal range expansion in a passerine bird. Oecologia 2011, 167:369-378.
90. Thompson C.K., Meitzen J., Replogle K., Drnevich J., Lent K.L., Wissman A.M., Farin F.M., Bammler T.K., Beyer R.P., Clayton D.F., et al. Seasonal changes in patterns of gene expression in avian song control brain regions. PLoS ONE 2012, 7:e35119.
91. Kuhn K., Schwenk K., Both C., Canal D., Johansson U.S., van der Mije S., Töpfer T., Päckert M. Differentiation in neutral genes and a candidate gene in the pied flycatcher: using biological archives to track global climate change. Ecol Evol 2013, 3:4799-4814.
92. Saino N., Bazzi G., Gatti E., Caprioli M., Cecere J.G., Possenti C.D., Galimberti A., Orioli V., Bani L., Rubolini D., et al. Polymorphism at the Clock gene predicts phenology of long-distance migration in birds. Mol Ecol 2015, 24:1758-1773.
93. Schoech S.J., Rensel M.A., Bridge E.S., Boughton R.K., Wilcoxen T.E. Environment, glucocorticoids, and the timing of reproduction. Gen Comp Endocrinol 2009, 163:201-207.
94. Moore I.T., Bonier F., Wingfield J.C. Reproductive asynchrony and population divergence between two tropical bird populations. Behav Ecol 2005, 16:755-762.
95. Helm B. Geographically distinct reproductive schedules in a changing world: costly implications in captive Stonechats. Integr Comp Biol 2009, 49:563-579.
96. Helm B. Zugunruhe of migratory and non-migratory birds in a circannual context. J Avian Biol 2006, 37:533-540.
97. Rayner M.J., Hauber M.E., Steeves T.E., Lawrence H.A., Thompson D.R., Sagar P.M., Bury S.J., Landers T.J., Phillips R.A., Ranjard L., et al. Contemporary and historical separation of transequatorial migration between genetically distinct seabird populations. Nat Commun 2011, 2:332.
98. Fort J., Steen H., Strom H., Tremblay Y., Gronningsaeter E., Pettex E., Porter W.P., Gremillet D. Energetic consequences of contrasting winter migratory strategies in a sympatric Arctic seabird duet. J Avian Biol 2013, 44:255-262.