Plant and animal populations can adapt to prolonged environmental changes if they have sufficient genetic variation in important phenological traits. The genetic regulation of annual cycles can be studied either via candidate genes or through the decomposition of phenotypic variance by quantitative genetics. Here, we combined both approaches to study the timing of migration in a long-distance migrant, the collared flycatcher (Ficedula albicollis). We found that none of the four studied candidate genes (CLOCK, NPAS2, ADCYAP1 and CREB1) had any consistent effect on the timing of six annual cycle stages of geolocator-tracked individuals. This negative result was confirmed by direct observations of males arriving in spring to the breeding site over four consecutive years. Although male spring arrival date was significantly repeatable (R = 0.24 ± 0.08 SE), most was attributable to permanent environmental effects, while the additive genetic variance and heritability were very low (h2 = 0.03 ± 0.17 SE). This low value constrains species evolutionary adaptation, and our study adds to warnings that such populations may be threatened, e.g. by ongoing climate change.

Department of Bird Migration Swiss Ornithological Institute Sempach Switzerland

Department of Zoology and Laboratory of Ornithology Faculty of Science Palacký University Olomouc Czech Republic

Department of Zoology Faculty of Science Charles University Prague Czech Republic

Lab of Ornithology Institute of Biology University of Latvia Salaspils Latvia

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Adamík P et al (2016) Barrier crossing in small avian migrants: individual tracking reveals prolonged nocturnal flights into the day as a common migratory strategy. Sci Rep. https://doi.org/10.1038/srep21560 PubMed DOI PMC

Ahola M, Laaksonen T, Sippola K, Eeva T, Rainio K, Lehikoinen E (2004) Variation in climate warming along the migration route uncouples arrival and breeding dates. Glob Change Biol 10:1610–1617. https://doi.org/10.1111/j.1365-2486.2004.00823.x DOI

Åkesson S, Ilieva M, Karagicheva J, Rakhimberdiev E, Tomotani B, Helm B (2017) Timing avian long-distance migration: from internal clock mechanisms to global flights. Philos Trans R Soc B Biol Sci 372:16. https://doi.org/10.1098/rstb.2016.0252 DOI

Alerstam T, Hake M, Kjellen N (2006) Temporal and spatial patterns of repeated migratory journeys by ospreys. Anim Behav 71:555–566. https://doi.org/10.1016/j.anbehav.2005.05.016 DOI

Arnaud CM, Becker PH, Dobson FS, Charmantier A (2013) Canalization of phenology in common terns: genetic and phenotypic variations in spring arrival date. Behav Ecol 24:683–690. https://doi.org/10.1093/beheco/ars214 DOI

Auld JR, Agrawal AA, Relyea RA (2010) Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc R Soc B Biol Sci 277:503–511. https://doi.org/10.1098/rspb.2009.1355 DOI

Bates D, Machler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01 DOI

Bazzi G et al (2015) Clock gene polymorphism and scheduling of migration: a geolocator study of the barn swallow Hirundo rustica. Sci Rep. https://doi.org/10.1038/srep12443 PubMed DOI PMC

Bazzi G et al (2017) Candidate genes have sex-specific effects on timing of spring migration and moult speed in a long-distance migratory bird. Curr Zool 63:479–486. https://doi.org/10.1093/cz/zow103 PubMed DOI

Bell-Pedersen D et al (2005) Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nat Rev Genet 6:544–556. https://doi.org/10.1038/nrg1633 PubMed DOI PMC

Both C (2010) Flexibility of timing of avian migration to climate change masked by environmental constraints en route. Curr Biol 20:243–248. https://doi.org/10.1016/j.cub.2009.11.074 PubMed DOI

Both C, Visser ME (2001) Adjustment to climate change is constrained by arrival date in a long-distance migrant bird. Nature 411:296–298. https://doi.org/10.1038/35077063 PubMed DOI

Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Climate change and population declines in a long-distance migratory bird. Nature 441:81–83. https://doi.org/10.1038/nature04539 PubMed DOI

Both C, Van Turnhout CAM, Bijlsma RG, Siepel H, Van Strien AJ, Foppen RPB (2010) Avian population consequences of climate change are most severe for long-distance migrants in seasonal habitats. Proc R Soc B Biol Sci 277:1259–1266. https://doi.org/10.1098/rspb.2009.1525 DOI

Both C, Bijlsma RG, Ouwehand J (2016) Repeatability in spring arrival dates in Pied Flycatchers varies among years and sexes. Ardea 104:3–21. https://doi.org/10.5253/arde.v104i1.a1 DOI

Bourret A, Garant D (2015) Candidate gene-environment interactions and their relationships with timing of breeding in a wild bird population. Ecol Evol 5:3628–3641. https://doi.org/10.1002/ece3.1630 PubMed DOI PMC

Briedis M et al (2016) Breeding latitude leads to different temporal but not spatial organization of the annual cycle in a long-distance migrant. J Avian Biol 47:743–748. https://doi.org/10.1111/jav.01002 DOI

Briedis M, Hahn S, Adamík P (2017) Cold spell en route delays spring arrival and decreases apparent survival in a long-distance migratory songbird. BMC Ecol. https://doi.org/10.1186/s12898-017-0121-4 PubMed DOI PMC

Briedis M, Hahn S, Krist M, Adamík P (2018) Finish with a sprint: evidence for time-selected last leg of migration in a long-distance migratory songbird. Ecol Evol 8:6899–6908. https://doi.org/10.1002/ece3.4206 PubMed DOI PMC

Briedis M et al (2019) A full annual perspective on sex-biased migration timing in long-distance migratory birds. Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2018.2821 DOI

Brlík V et al (2020) Weak effects of geolocators on small birds: a meta-analysis controlled for phylogeny and publication bias. J Anim Ecol 89:207–220. https://doi.org/10.1111/1365-2656.12962 PubMed DOI

Butler D (2009) Asreml() fits the linear mixed model. R package version 3.0

Caprioli M et al (2012) Clock gene variation is associated with breeding phenology and maybe under directional selection in the migratory barn swallow. PLoS ONE. https://doi.org/10.1371/journal.pone.0035140 PubMed DOI PMC

Chakarov N, Jonker RM, Boerner M, Hoffman JI, Kruger O (2013) Variation at phenological candidate genes correlates with timing of dispersal and plumage morph in a sedentary bird of prey. Mol Ecol 22:5430–5440. https://doi.org/10.1111/mec.12493 PubMed DOI

Charmantier A, Gienapp P (2014) Climate change and timing of avian breeding and migration: evolutionary versus plastic changes. Evol Appl 7:15–28. https://doi.org/10.1111/eva.12126 PubMed DOI

Charmantier A, Reale D (2005) How do misassigned paternities affect the estimation of heritability in the wild? Mol Ecol 14:2839–2850. https://doi.org/10.1111/j.1365-294X.2005.02619.x PubMed DOI

Charmantier A, McCleery RH, Cole LR, Perrins C, Kruuk LEB, Sheldon BC (2008) Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320:800–803. https://doi.org/10.1126/science.1157174 PubMed DOI

Chevin LM, Lande R, Mace GM (2010) Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLOS Biol 8:8. https://doi.org/10.1371/journal.pbio.1000357 DOI

Clark RG, Poysa H, Runko P, Paasivaara A (2014) Spring phenology and timing of breeding in short-distance migrant birds: phenotypic responses and offspring recruitment patterns in common goldeneyes. J Avian Biol 45:457–465. https://doi.org/10.1111/jav.00290 DOI

Conklin JR, Battley PF, Potter MA (2013) Absolute consistency: individual versus population variation in annual-cycle schedules of a long-distance migrant bird. PLoS ONE 8:9. https://doi.org/10.1371/journal.pone.0054535 DOI

Contina A, Bridge ES, Ross JD, Shipley JR, Kelly JF (2018) Examination of Clock and Adcyap1 gene variation in a neotropical migratory passerine. PLoS ONE. https://doi.org/10.1371/journal.pone.0190859 PubMed DOI PMC

DeBruyne JP, Weaver DR, Reppert SM (2007) CLOCK and NPAS2 have overlapping roles in the suprachiasmatic circadian clock. Nat Neurosci 10:543–545. https://doi.org/10.1038/nn1884 PubMed DOI PMC

Delmore KE, Toews DPL, Germain RR, Owens GL, Irwin DE (2016) The genetics of seasonal migration and plumage color. Curr Biol 26:2167–2173. https://doi.org/10.1016/j.cub.2016.06.015 PubMed DOI

DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81. https://doi.org/10.1016/s0169-5347(97)01274-3 PubMed DOI

Dohm MR (2002) Repeatability estimates do not always set an upper limit to heritability. Funct Ecol 16:273–280 DOI

Dor R et al (2012) Clock gene variation in Tachycineta swallows. Ecol Evol 2:95–105. https://doi.org/10.1002/ece3.73 PubMed DOI PMC

Dunlap JC (1999) Molecular bases for circadian clocks. Cell 96:271–290. https://doi.org/10.1016/s0092-8674(00)80566-8 PubMed DOI

Edme A et al (2017) Do ornaments, arrival date, and sperm size influence mating and paternity success in the collared flycatcher? Behav Ecol Sociobiol. https://doi.org/10.1007/s00265-016-2242-8 DOI

Edme A, Zobač P, Korsten P, Albrecht T, Schmoll T, Krist M (2019) Moderate heritability and low evolvability of sperm morphology in a species with high risk of sperm competition, the collared flycatcher Ficedula albicollis. J Evol Biol 32:205–217. https://doi.org/10.1111/jeb.13404 PubMed DOI

Falconer DS (1993) Introduction to quantitative genetics. Longman Scientific & Technical, Essex

Firth JA, Hadfield JD, Santure AW, Slate J, Sheldon BC (2015) The influence of nonrandom extra-pair paternity on heritability estimates derived from wild pedigrees. Evolution 69:1336–1344. https://doi.org/10.1111/evo.12649 PubMed DOI PMC

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. https://doi.org/10.1016/j.tree.2004.11.017 PubMed DOI

Fraser KC, Shave A, de Greef E, Siegrist J, Garroway CJ (2019) Individual variability in migration timing can explain long-term, population-level advances in a songbird. Front Ecol Evol 7:7. https://doi.org/10.3389/fevo.2019.00324 DOI

Gienapp P, Brommer JE (2014) Evolutionary dynamics in response to climate change. In: Charmantier A, Garant D, Kruuk LEB (eds) Quantitative genetics in the wild. Oxford University Press, Oxford, pp 254–273 DOI

Gienapp P, Lof M, Reed TE, McNamara J, Verhulst S, Visser ME (2013) Predicting demographically sustainable rates of adaptation: can great tit breeding time keep pace with climate change? Philos Trans R Soc B Biol Sci 368:10. https://doi.org/10.1098/rstb.2012.0289 DOI

Gienapp P, Laine VN, Mateman AC, van Oers K, Visser ME (2017) Environment-dependent genotype-phenotype associations in avian breeding time. Front Genet. https://doi.org/10.3389/fgene.2017.00102 PubMed DOI PMC

Gwinner E (1996) Circadian and circannual programmes in avian migration. J Exp Biol 199:39–48 DOI

Haest B, Hüppop O, Bairlein F (2020) Weather at the winter and stopover areas determines spring migration onset, progress, and advancements in Afro-Palearctic migrant birds. Proc Natl Acad Sci USA 117:17056–17062. https://doi.org/10.1073/pnas.1920448117 PubMed DOI PMC

Hannibal J et al (1997) Pituitary adenylate cyclase-activating peptide (PACAP) in the retinohypothalamic tract: a potential daytime regulator of the biological clock. J Neurosci 17:2637–2644. https://doi.org/10.1523/jneurosci.17-07-02637.1997 PubMed DOI PMC

Hasselquist D, Montras-Janer T, Tarka M, Hansson B (2017) Individual consistency of long-distance migration in a songbird: significant repeatability of autumn route, stopovers and wintering sites but not in timing of migration. J Avian Biol 48:91–102. https://doi.org/10.1111/jav.01292 DOI

Helm B et al (2013) Annual rhythms that underlie phenology: biological time-keeping meets environmental change. Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2013.0016 DOI

Helm B, Van Doren BM, Hoffmann D, Hoffmann U (2019) Evolutionary response to climate change in migratory pied flycatchers. Curr Biol 29:3714. https://doi.org/10.1016/j.cub.2019.08.072 PubMed DOI

Hill WG, Goddard ME, Visscher PM (2008) Data and theory point to mainly additive genetic variance for complex traits. PLOS Genet 4:10. https://doi.org/10.1371/journal.pgen.1000008 DOI

Hüppop O, Winkel W (2006) Climate change and timing of spring migration in the long-distance migrant Ficedula hypoleuca in central Europe: the role of spatially different temperature changes along migration routes. J Orn 147:344–353. https://doi.org/10.1007/s10336-005-0049-x DOI

Johnsen A et al (2007) Avian Clock gene polymorphism: evidence for a latitudinal cline in allele frequencies. Mol Ecol 16:4867–4880. https://doi.org/10.1111/j.1365-294X.2007.03552.x PubMed DOI

Kako K, Ishida N (1998) The role of transcription factors in circadian gene expression. Neurosci Res 31:257–264. https://doi.org/10.1016/s0168-0102(98)00054-6 PubMed DOI

Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106. https://doi.org/10.1111/j.1365-294X.2007.03089.x DOI

Klvaňa P, Cepák J, Munclinger P, Michálková R, Tomášek O, Albrecht T (2018) Around the Mediterranean: an extreme example of loop migration in a long-distance migratory passerine. J Avian Biol 49:e01595. https://doi.org/10.1111/jav.01595 DOI

Koleček J, Adamík P, Reif J (2020) Shifts in migration phenology under climate change: temperature vs. abundance effects in birds. Clim Change. https://doi.org/10.1007/s10584-020-02668-8 DOI

Krist M, Munclinger P (2011) Superiority of extra-pair offspring: maternal but not genetic effects as revealed by a mixed cross-fostering design. Mol Ecol 20:5074–5091. https://doi.org/10.1111/j.1365-294X.2011.05337.x PubMed DOI

Krist M, Nádvorník P, Uvírová L, Bureš S (2005) Paternity covaries with laying and hatching order in the collared flycatcher Ficedula albicollis. Behav Ecol Sociobiol 59:6–11. https://doi.org/10.1007/s00265-005-0002-2 DOI

Kyriacou CP, Peixoto AA, Sandrelli F, Costa R, Tauber E (2008) Clines in clock genes: fine-tuning circadian rhythms to the environment. Trends Genet 24:124–132. https://doi.org/10.1016/j.tig.2007.12.003 PubMed DOI

Lehikoinen A et al (2019) Phenology of the avian spring migratory passage in Europe and North America: asymmetric advancement in time and increase in duration. Ecol Indic 101:985–991. https://doi.org/10.1016/j.ecolind.2019.01.083 DOI

Liedvogel M, Sheldon BC (2010) Low variability and absence of phenotypic correlates of Clock gene variation in a great tit Parus major population. J Avian Biol 41:543–550. https://doi.org/10.1111/j.1600-048X.2010.05055.x DOI

Liedvogel M, Szulkin M, Knowles SCL, Wood MJ, Sheldon BC (2009) Phenotypic correlates of Clock gene variation in a wild blue tit population: evidence for a role in seasonal timing of reproduction. Mol Ecol 18:2444–2456. https://doi.org/10.1111/j.1365-294X.2009.04204.x PubMed DOI

Liedvogel M, Akesson S, Bensch S (2011) The genetics of migration on the move. Trends Ecol Evol 26:561–569. https://doi.org/10.1016/j.tree.2011.07.009 PubMed DOI

Liedvogel M, Cornwallis CK, Sheldon BC (2012) Integrating candidate gene and quantitative genetic approaches to understand variation in timing of breeding in wild tit populations. J Evol Biol 25:813–823. https://doi.org/10.1111/j.1420-9101.2012.02480.x PubMed DOI

Lisovski S, Hahn S (2012) GeoLight-processing and analysing light-based geolocator data in R. Methods Ecol Evol 3:1055–1059. https://doi.org/10.1111/j.2041-210X.2012.00248.x DOI

Lisovski S et al (2020) Light-level geolocator analyses: a user’s guide. J Anim Ecol 89:221–236. https://doi.org/10.1111/1365-2656.13036 PubMed DOI

Lisovski S et al (2021) The Indo-European flyway: opportunities and constraints reflected by Common Rosefinches breeding across Europe. J Biogeogr. https://doi.org/10.1111/jbi.14085 DOI

Lonze BE, Ginty DD (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron 35:605–623. https://doi.org/10.1016/s0896-6273(02)00828-0 PubMed DOI

Lopez-Lopez P, Garcia-Ripolles C, Urios V (2014) Individual repeatability in timing and spatial flexibility of migration routes of trans-Saharan migratory raptors. Curr Zool 60:642–652. https://doi.org/10.1093/czoolo/60.5.642 DOI

Lourenco PM, Kentie R, Schroeder J, Groen NM, Hooijmeijer J, Piersma T (2011) Repeatable timing of northward departure, arrival and breeding in Black-tailed Godwits Limosa l. limosa, but no domino effects. J Orn 152:1023–1032. https://doi.org/10.1007/s10336-011-0692-3 DOI

Lundberg M et al (2017) Genetic differences between willow warbler migratory phenotypes are few and cluster in large haplotype blocks. Evol Lett 1:155–168. https://doi.org/10.1002/evl3.15 PubMed DOI PMC

Merlin C, Liedvogel M (2019) The genetics and epigenetics of animal migration and orientation: birds, butterflies and beyond. J Exp Biol. https://doi.org/10.1242/jeb.191890 PubMed DOI

Møller AP (2001) Heritability of arrival date in a migratory bird. Proc R Soc B Biol Sci 268:203–206 DOI

Møller AP, Rubolini D, Lehikoinen E (2008) Populations of migratory bird species that did not show a phenological response to climate change are declining. Proc Natl Acad Sci USA 105:16195–16200. https://doi.org/10.1073/pnas.0803825105 PubMed DOI PMC

Mueller JC, Pulido F, Kempenaers B (2011) Identification of a gene associated with avian migratory behaviour. Proc R Soc B Biol Sci 278:2848–2856. https://doi.org/10.1098/rspb.2010.2567 DOI

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. https://doi.org/10.1016/j.peptides.2007.07.013 PubMed DOI

O’Malley KG, Ford MJ, Hard JJ (2010) Clock polymorphism in Pacific salmon: evidence for variable selection along a latitudinal gradient. Proc R Soc B Biol Sci 277:3703–3714. https://doi.org/10.1098/rspb.2010.0762 DOI

Ouwehand J, Both C (2017) African departure rather than migration speed determines variation in spring arrival in pied flycatchers. J Anim Ecol 86:88–97. https://doi.org/10.1111/1365-2656.12599 PubMed DOI

Parody-Merino AM, Battley PF, Conklin JR, Fidler AE (2019) No evidence for an association between Clock gene allelic variation and migration timing in a long-distance migratory shorebird (Limosa lapponica baueri). Oecologia 191:843–859. https://doi.org/10.1007/s00442-019-04524-8 PubMed DOI

Pearce-Higgins J, Green R (2014) Birds and climate change: impacts and conservation responses. Cambridge University Press, Cambridge DOI

Peterson MP, Abolins-Abols M, Atwell JW, Rice RJ, Milá B, Ketterson ED (2013) Variation in candidate genes CLOCK and ADCYAP1 does not consistently predict differences in migratory behavior in the songbird genus Junco. F1000Research 2:17 DOI

Portugal SJ, White CR (2018) Miniaturisation of biologgers is not alleviating the 5% rule. Methods Ecol Evol 9:1662–1666. https://doi.org/10.1111/2041-210X.13013 DOI

Potti J (1998) Arrival time from spring migration in male Pied Flycatchers: individual consistency and familial resemblance. Condor 100:702–708. https://doi.org/10.2307/1369752 DOI

Pulido F (2007a) Phenotypic changes in spring arrival: evolution, phenotypic plasticity, effects of weather and condition. Clim Res 35:5–23. https://doi.org/10.3354/cr00711 DOI

Pulido F (2007b) The genetics and evolution of avian migration. Bioscience 57:165–174. https://doi.org/10.1641/b570211 DOI

Pulido F, Berthold P, Mohr G, Querner U (2001) Heritability of the timing of autumn migration in a natural bird population. Proc R Soc B Biol Sci 268:953–959. https://doi.org/10.1098/rspb.2001.1602 DOI

Radchuk V et al (2019) Adaptive responses of animals to climate change are most likely insufficient. Nat Commun. https://doi.org/10.1038/s41467-019-10924-4 PubMed DOI PMC

Ralston J et al (2019) Length polymorphisms at two candidate genes explain variation of migratory behaviors in blackpoll warblers (Setophaga striata). Ecol Evol 9:8840–8855. https://doi.org/10.1002/ece3.5436 PubMed DOI PMC

Ramos JSL, Delmore KE, Liedvogel M (2017) Candidate genes for migration do not distinguish migratory and non-migratory birds. J Comp Physiol A Neuroethol 203:383–397. https://doi.org/10.1007/s00359-017-1184-6 DOI

Reick M, Garcia JA, Dudley C, McKnight SL (2001) NPAS2: an analog of clock operative in the mammalian forebrain. Science 293:506–509. https://doi.org/10.1126/science.1060699 PubMed DOI

Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225. https://doi.org/10.2307/2409177 PubMed DOI

Romano A et al (2018) Circadian genes polymorphism and breeding phenology in a resident bird, the yellow-legged gull. J Zool 304:117–123. https://doi.org/10.1111/jzo.12501 DOI

Rosivall B, Szöllösi E, Hasselquist D, Török J (2009) Effects of extrapair paternity and sex on nestling growth and condition in the collared flycatcher, Ficedula albicollis. Anim Behav 77:611–617. https://doi.org/10.1016/j.anbehav.2008.11.009 DOI

Rubolini D, Møller AP, Rainio K, Lehikoinen E (2007) Intraspecific consistency and geographic variability in temporal trends of spring migration phenology among European bird species. Clim Res 35:135–146. https://doi.org/10.3354/cr00720 DOI

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. Glob Change Biol 14:250–263. https://doi.org/10.1111/j.1365-2486.2007.01488.x DOI

Saino N et al (2013) Timing of molt of barn swallows is delayed in a rare Clock genotype. PeerJ. https://doi.org/10.7717/peerj.17 PubMed DOI PMC

Saino N et al (2017) Migration phenology and breeding success are predicted by methylation of a photoperiodic gene in the barn swallow. Sci Rep. https://doi.org/10.1038/srep45412 PubMed DOI PMC

Schmaljohann H (2019) The start of migration correlates with arrival timing, and the total speed of migration increases with migration distance in migratory songbirds: a cross-continental analysis. Mov Ecol. https://doi.org/10.1186/s40462-019-0169-1 PubMed DOI PMC

Sergio F et al (2014) Individual improvements and selective mortality shape lifelong migratory performance. Nature 515:410–413. https://doi.org/10.1038/nature13696 PubMed DOI

Sheldon BC, Ellegren H (1999) Sexual selection resulting from extrapair paternity in collared flycatchers. Anim Behav 57:285–298. https://doi.org/10.1006/anbe.1998.0968 PubMed DOI

Sherwood NM, Krueckl SL, McRory JE (2000) The origin and function of the pituitary adenylate cyclase-activating polypeptide (PACAP)/glucagon superfamily. Endocr Rev 21:619–670. https://doi.org/10.1210/er.21.6.619 PubMed DOI

Silva AJ, Kogan JH, Frankland PW, Kida S (1998) CREB and memory. Annu Rev Neurosci 21:127–148. https://doi.org/10.1146/annurev.neuro.21.1.127 PubMed DOI

Stanley CQ, MacPherson M, Fraser KC, McKinnon EA, Stutchbury BJM (2012) Repeat tracking of individual songbirds reveals consistent migration timing but flexibility in route. PLoS ONE 7:6. https://doi.org/10.1371/J.pone.0040688 DOI

Stapley J et al (2010) Adaptation genomics: the next generation. Trends Ecol Evol 25:705–712. https://doi.org/10.1016/j.tree.2010.09.002 PubMed DOI

Steinmeyer C, Mueller JC, Kempenaers B (2009) Search for informative polymorphisms in candidate genes: clock genes and circadian behaviour in blue tits. Genetica 136:109–117. https://doi.org/10.1007/s10709-008-9318-y PubMed DOI

Stoffel MA, Nakagawa S, Schielzeth H (2017) rptR: repeatability estimation and variance decomposition by generalized linear mixed-effects models. Methods Ecol Evol 8:1639–1644. https://doi.org/10.1111/2041-210x.12797 DOI

Tarka M, Hansson B, Hasselquist D (2015) Selection and evolutionary potential of spring arrival phenology in males and females of a migratory songbird. J Evol Biol 28:1024–1038. https://doi.org/10.1111/jeb.12638 PubMed DOI

Team RC (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

Teplitsky C, Mouawad NG, Balbontin J, de Lope F, Møller AP (2011) Quantitative genetics of migration syndromes: a study of two barn swallow populations. J Evol Biol 24:2025–2039. https://doi.org/10.1111/j.1420-9101.2011.02342.x PubMed DOI

Toews DPL, Taylor SA, Streby HM, Kramer GR, Lovette IJ (2019) Selection on VPS13A linked to migration in a songbird. Proc Natl Acad Sci USA 116:18272–18274. https://doi.org/10.1073/pnas.1909186116 PubMed DOI PMC

Tomotani BM et al (2018) Climate change leads to differential shifts in the timing of annual cycle stages in a migratory bird. Glob Change Biol 24:823–835. https://doi.org/10.1111/gcb.14006 DOI

Usui T, Butchart SHM, Phillimore AB (2017) Temporal shifts and temperature sensitivity of avian spring migratory phenology: a phylogenetic meta-analysis. J Anim Ecol 86:250–261. https://doi.org/10.1111/1365-2656.12612 PubMed DOI

van Wijk RE, Bauer S, Schaub M (2016) Repeatability of individual migration routes, wintering sites, and timing in a long-distance migrant bird. Ecol Evol 6:8679–8685. https://doi.org/10.1002/ece3.2578 PubMed DOI PMC

Vardanis Y, Klaassen RHG, Strandberg R, Alerstam T (2011) Individuality in bird migration: routes and timing. Biol Lett 7:502–505. https://doi.org/10.1098/rsbl.2010.1180 PubMed DOI PMC

Vedder O, Bouwhuis S, Sheldon BC (2013) Quantitative assessment of the importance of phenotypic plasticity in adaptation to climate change in wild bird populations. PLOS Biol 11:10. https://doi.org/10.1371/J.pbio.1001605 DOI

Verhagen I et al (2019) Genetic and phenotypic responses to genomic selection for timing of breeding in a wild songbird. Funct Ecol 33:1708–1721. https://doi.org/10.1111/1365-2435.13360 DOI

Visser ME, Caro SP, van Oers K, Schaper SV, Helm B (2010) Phenology, seasonal timing and circannual rhythms: towards a unified framework. Philos Trans R Soc B Biol Sci 365:3113–3127. https://doi.org/10.1098/rstb.2010.0111 DOI

Weidinger K, Král M (2007) Climatic effects on arrival and laying dates in a long-distance migrant, the Collared Flycatcher Ficedula albicollis. Ibis 149:836–847. https://doi.org/10.1111/j.1474-919X.2007.00719.x DOI

Wilson AJ et al (2010) An ecologist’s guide to the animal model. J Anim Ecol 79:13–26. https://doi.org/10.1111/j.1365-2656.2009.01639.x PubMed DOI PMC

Wolak ME (2012) nadiv: an R package to create relatedness matrices for estimating non-additive genetic variances in animal models. Methods Ecol Evol 3:792–796 DOI

Wolak K, Keller F (2014) Dominance genetic variance and inbreeding in natural populations. In: Charmantier A, Garant D, Kruuk LEB (eds) Quantitative genetics in the wild. Oxford University Press, Oxford, pp 104–127 DOI