Brain gene expression reveals pathways underlying nocturnal migratory restlessness

Bairlein, F. How to get fat: nutritional mechanisms of seasonal fat accumulation in migratory songbirds. Naturwissenschaften. 89, 1–10. https://doi.org/10.1007/s00114-001-0279-6 (2002).Article 
ADS 
PubMed 

Google Scholar 
Berthold, P. Evolutionary aspects of migratory behavior in European warblers. J. Evol. Biol.1, 195–209. https://doi.org/10.1046/j.1420-9101.1998.1030195.x (1988).Article 

Google Scholar 
Piersma, T., Perez-Tris, J., Mouritsen, H., Bauchinger, U. & Bairlein, F. Is there a migratory syndrome common to all migrant birds? Ann. N Y Acad. Sci.1046, 282–293. https://doi.org/10.1196/annals.1343.026 (2005).Article 
ADS 
PubMed 

Google Scholar 
Newton, I. Bird MigrationHarperCollins,. (2010).Guglielmo, C. G. Obese super athletes: fat-fueled migration in birds and bats. J. Exp. Biol.221, jeb165753. https://doi.org/10.1242/jeb.165753 (2018).Article 
PubMed 

Google Scholar 
Rattenborg, N. C. et al. Migratory sleeplessness in the White-Crowned Sparrow (Zonotrichia leucophrys gambelii). PLoS Biol.2, e212. https://doi.org/10.1371/journal.pbio.0020212 (2004).Article 
PubMed 
PubMed Central 

Google Scholar 
Berthold, P. Control of bird Migration (Chapman & Hall, 1996).Gwinner, E. in In Adv. Stud. Behav. Vol. 16, 191–228 (eds Rosenblatt, J. S., Beer, C., Busnel, M. C. & Slater, P. J. B.) (Academic, 1986).Lupi, S., Slezacek, J. & Fusani, L. The physiology of stopover decisions: food, fat and zugunruhe on a Mediterranean island. J. Ornithol.160, 1205–1212. https://doi.org/10.1007/s10336-019-01693-4 (2019).Article 

Google Scholar 
Gwinner, E. in In Bird Migration. Physiology and Ecophysiology. 257–268 (eds Gwinner, E.) (Springer, 1990).Helm, B. & Gwinner, E. Migratory restlessness in an equatorial nonmigratory bird. PLoS Biol.4, e110. https://doi.org/10.1371/journal.pbio.0040110 (2006).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Williams, B. K., Nichols, J. D. & Conroy, M. J. Analysis and Management of Animal Populations. Modeling, Estimation, and Decision Making (Academic, 2002).Helbig, A. J. Inheritance of migratory direction in a bird species: a cross-breeding experiment with SE- and SW-migrating blackcaps (Sylvia atricapilla). Behav. Ecol. Sociobiol.28, 9–12 (1991).Article 

Google Scholar 
Derégnaucourt, S., Guyomarc’h, J. C. & Spanò, S. Behavioural evidence of hybridization (Japanese×European) in domestic quail released as game birds. Appl. Anim. Behav. Sci.94, 303–318. https://doi.org/10.1016/j.applanim.2005.03.002 (2005).Article 

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

Google Scholar 
Mueller, J. C., Pulido, F. & Kempenaers, B. Identification of a gene associated with avian migratory behaviour. Proceedings of the Royal Society B-Biological Sciences 278, 2848–2856, doi: (2011). https://doi.org/10.1098/rspb.2010.2567Saino, N. et al. Polymorphism at the clock gene predicts phenology of long-distance migration in birds. Mol. Ecol.24, 1758–1773. https://doi.org/10.1111/mec.13159 (2015).Article 
CAS 
PubMed 

Google Scholar 
Sanchez-Donoso, I. et al. Massive genome inversion drives coexistence of divergent morphs in common quails. Curr. Biol.32, 462–469e466. https://doi.org/10.1016/j.cub.2021.11.019 (2022).Article 
CAS 
PubMed 

Google Scholar 
Sokolovskis, K. et al. Migration direction in a songbird explained by two loci. Nat. Commun.14, 165. https://doi.org/10.1038/s41467-023-35788-7 (2023).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Gu, Z. et al. Climate-driven flyway changes and memory-based long-distance migration. Nature. 591, 259–264. https://doi.org/10.1038/s41586-021-03265-0 (2021).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Pulido, F., Berthold, P. & van Noordwijk, A. J. Frequency of migrants and migratory activity are genetically correlated in a bird population: Evolutionary implications. Proc. Natl. Acad. Sci. USA 93, 14642–14647 (1996).Cornelius, J. M., Boswell, T., Jenni-Eiermann, S., Breuner, C. W. & Ramenofsky, M. Contributions of endocrinology to the migration life history of birds. Gen. Comp. Endocrinol.190, 47–60. https://doi.org/10.1016/j.ygcen.2013.03.027 (2013).Article 
CAS 
PubMed 

Google Scholar 
Boswell, T. & Dunn, I. C. Regulation of Agouti-related protein and Pro-opiomelanocortin Gene expression in the Avian Arcuate Nucleus. Front. Endocrinol.8https://doi.org/10.3389/fendo.2017.00075 (2017).Frias-Soler, R. C., Pildaín, L. V., Pârâu, L. G., Wink, M. & Bairlein, F. Transcriptome signatures in the brain of a migratory songbird. Comp. Biochem. Physiol. D: Genomics Proteomics. 34, 100681. https://doi.org/10.1016/j.cbd.2020.100681 (2020).Article 
CAS 
PubMed 

Google Scholar 
Johnston, R. A., Paxton, K. L., Moore, F. R., Wayne, R. K. & Smith, T. B. Seasonal gene expression in a migratory songbird. Mol. Ecol.25, 5680–5691. https://doi.org/10.1111/mec.13879 (2016).Article 
CAS 
PubMed 

Google Scholar 
Sharma, A. et al. Photoperiodically driven transcriptome-wide changes in the hypothalamus reveal transcriptional differences between physiologically contrasting seasonal life-history states in migratory songbirds. Sci. Rep.11, 12823. https://doi.org/10.1038/s41598-021-91951-4 (2021).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Boss, J. et al. Gene expression in the brain of a migratory songbird during breeding and migration. Mov. Ecol.4. https://doi.org/10.1186/s40462-016-0069-6 (2016).Marasco, V., Herzyk, P., Robinson, J. & Spencer, K. A. Pre- and post-natal stress programming: developmental exposure to glucocorticoids causes long-term brain-region specific changes to Transcriptome in the precocial Japanese quail. J. Neuroendocrinol.28. https://doi.org/10.1111/jne.12387 (2016).Naurin, S., Hansson, B., Hasselquist, D., Kim, Y. H. & Bensch, S. The sex-biased brain: sexual dimorphism in gene expression in two species of songbirds. BMC Genom.12, 37. https://doi.org/10.1186/1471-2164-12-37 (2011).Article 

Google Scholar 
Patchett, R., Kirschel, A. N. G., King, R., Styles, J., Cresswell, W. & P. & Age-related changes in migratory behaviour within the first annual cycle of a passerine bird. PLoS ONE. 17, e0273686. https://doi.org/10.1371/journal.pone.0273686 (2022).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Boswell, T., Hall, M. R. & Goldsmith, A. R. Annual cycles of migratory fattening, reproduction and moult in European quail (Coturnix coturnix). J. Zool.231, 627–644. https://doi.org/10.1111/j.1469-7998.1993.tb01943.x (1993).Article 

Google Scholar 
Marasco, V., Sebastiano, M., Costantini, D., Pola, G. & Fusani, L. Controlled expression of the migratory phenotype affects oxidative status in birds. J. Exp. Biol.224, jeb233486. https://doi.org/10.1242/jeb.233486 (2021).Article 
PubMed 

Google Scholar 
Marasco, V., Kaiya, H., Pola, G. & Fusani, L. Ghrelin, not corticosterone, is associated with transitioning of phenotypic states in a migratory Galliform. Front. Endocrinol.13, 1058298. https://doi.org/10.3389/fendo.2022.1058298 (2023).Article 

Google Scholar 
Robinson, J. E. & Follett, B. K. Photoperiodism in Japanese quail: the termination of Seasonal breeding by Photorefractoriness. Proc. Royal Soc. Lond. Ser. B Biol. Sci.215, 95–116 (1982).ADS 
CAS 

Google Scholar 
Marasco, V., Sebastiano, M., Costantini, D., Pola, G. & Fusani, L. Controlled expression of the migratory phenotype affects oxidative status in birds. The Journal of Experimental Biology, jeb.233486, doi: (2021). https://doi.org/10.1242/jeb.233486Smith, S., Fusani, L., Boglarka, B., Sanchez-Donoso, I. & Marasco, V. Lack of introgression of Japanese quail in a captive population of common quail. Eur. J. Wildl. Res.64, 51. https://doi.org/10.1007/s10344-018-1209-7 (2018).Article 

Google Scholar 
Ouyang, J. Q., Davies, S. & Dominoni, D. Hormonally mediated effects of artificial light at night on behavior and fitness: linking endocrine mechanisms with function. J. Exp. Biol.221https://doi.org/10.1242/jeb.156893 (2018).Sachs, B. D. Photoperiodic control of reproductive behavior and physiology of the male Japanese quail (Coturnix coturnix japonica). Horm. Behav.1, 7–24. https://doi.org/10.1016/0018-506X(69)90002-6 (1969).Article 

Google Scholar 
DERÉGNAUCOURT, S., GUYOMARC’H, J. C. & BELHAMRA, M. Comparison of migratory tendency in European quail Coturnix c. coturnix, domestic Japanese quail Coturnix c. Japonica and their hybrids. Ibis. 147, 25–36. https://doi.org/10.1111/j.1474-919x.2004.00313.x (2005).Article 

Google Scholar 
Marasco, V., Fusani, L., Pola, G. & Smith, S. Data on the de novo transcriptome assembly for the migratory bird, the common quail (Coturnix coturnix). Data Brief.32, 106041. https://doi.org/10.1016/j.dib.2020.106041 (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
Puelles, L., Martinez-de-la-Torre, M., Paxinos, G., Watson, C. & Martinez, S. The Chick Brain in Stereotaxic Coordinates: An Atlas Featuring Neuromeric Subdivisions and Mammalian Homologies (Academic, 2007).Lessells, C. M. & Boag, P. T. Unrepeatable repeatabilities – A Common Mistake. Auk. 104, 116–121 (1987).Article 

Google Scholar 
Bertin, A., Houdelier, C., Richard-Yris, M. A., Guyomarc’h, C. & Lumineau, S. Stable individual profiles of daily timing of migratory restlessness in European quail. Chronobiol Int.24, 253–267. https://doi.org/10.1080/07420520701283685 (2007).Article 
PubMed 

Google Scholar 
Zúñiga, D. et al. Abrupt switch to migratory night flight in a wild migratory songbird. Sci. Rep.6, 34207. https://doi.org/10.1038/srep34207 (2016).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Chen, T. H., Gross, J. A. & Karasov, W. H. Chronic exposure to pentavalent arsenic of larval leopard frogs (Rana pipiens): bioaccumulation and reduced swimming performance. Ecotoxicology. 18, 587–593. https://doi.org/10.1007/S10646-009-0316-3 (2009).Article 
PubMed 

Google Scholar 
Bryant, D. M. et al. A tissue-mapped Axolotl De Novo Transcriptome enables identification of limb regeneration factors. Cell. Rep.18, 762–776. https://doi.org/10.1016/j.celrep.2016.12.063 (2017).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Powell, S. et al. eggNOG v3.0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges. Nucleic Acids Res.40, D284–D289. https://doi.org/10.1093/nar/gkr1060 (2012).Article 
CAS 
PubMed 

Google Scholar 
Conesa, A. et al. A survey of best practices for RNA-seq data analysis. Genome Biol.17https://doi.org/10.1186/s13059-016-0881-8 (2016).Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 30, 2114–2120. https://doi.org/10.1093/bioinformatics/btu170 (2014).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Bray, N. L., Pimentel, H., Melsted, P. & Pachter, L. Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol.34, 525–527. https://doi.org/10.1038/nbt.3519 (2016).Article 
CAS 
PubMed 

Google Scholar 
Love, M. I., Huber, W. & Anders, S. Moderated estimation of Fold change and dispersion for RNA-seq data with DESeq2. Genome Biol.15, 550. https://doi.org/10.1186/s13059-014-0550-8 (2014).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Benjamini, Y. & Hochberg, Y. Controlling the false Discovery rate: a practical and powerful Approach to multiple testing. J. R Stat. Soc. B. 57, 289–300. https://doi.org/10.2307/2346101 (1995).Article 
MathSciNet 

Google Scholar 
R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, (2022).RStudio & RStudio Integrated Development for R (PBC, Boston, MA, (2023).emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.8.9. (2023).Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A. & Smith, G. M. Mixed Efffects Models and Extensions in Ecology with R. I-XXII, 1-574; Index (Springer, 2009).Sharma, A., Singh, D., Das, S. & Kumar, V. Hypothalamic and liver transcriptome from two crucial life-history stages in a migratory songbird. Exp. Physiol.103, 559–569. https://doi.org/10.1113/EP086831 (2018).Article 
CAS 
PubMed 

Google Scholar 
Singh, D., Swarup, V., Le, H. & Kumar, V. Transcriptional Signatures in liver reveal metabolic adaptations to Seasons in Migratory Blackheaded Buntings. Front. Physiol.9, 1568. https://doi.org/10.3389/fphys.2018.01568 (2018).Article 
PubMed 
PubMed Central 

Google Scholar 
Frias-Soler, R. C., Kelsey, N. A., Villarín Pildaín, L., Wink, M. & Bairlein, F. Transcriptome signature changes in the liver of a migratory passerine. Genomics. 114, 110283. https://doi.org/10.1016/j.ygeno.2022.110283 (2022).Article 
CAS 
PubMed 

Google Scholar 
Horton, W. J. et al. Transcriptome analyses of Heart and Liver Reveal Novel pathways for regulating Songbird Migration. Sci. Rep.9, 6058. https://doi.org/10.1038/s41598-019-41252-8 (2019).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Guglielmo, C. G. Move that fatty acid: fuel selection and transport in migratory birds and bats. Integr. Comp. Biol.50, 336–345. https://doi.org/10.1093/icb/icq097 (2010).Article 
PubMed 

Google Scholar 
Elliott, D. A., Weickert, C. S. & Garner, B. Apolipoproteins in the brain: implications for neurological and psychiatric disorders. Clin. Lipidol.5, 555–573. https://doi.org/10.2217/clp.10.37 (2010).Article 
CAS 

Google Scholar 
Mather, K. A. et al. Genome-wide significant results identified for plasma apolipoprotein H levels in middle-aged and older adults. Sci. Rep.6, 23675. https://doi.org/10.1038/srep23675 (2016).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Mahley, R. W. & Apolipoprotein, E. Cholesterol Transport Protein with Expanding Role in Cell Biology. Science. 240, 622–630. https://doi.org/10.1126/science.3283935 (1988).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Koch, S. et al. Characterization of four lipoprotein classes in human cerebrospinal fluid. J. Lipid Res.42, 1143–1151. https://doi.org/10.1016/S0022-2275(20)31605-9 (2001).Article 
CAS 
PubMed 

Google Scholar 
Castro, A. et al. APOH is increased in the plasma and liver of type 2 diabetic patients with metabolic syndrome. Atherosclerosis. 209, 201–205. https://doi.org/10.1016/j.atherosclerosis.2009.09.072 (2010).Article 
CAS 
PubMed 

Google Scholar 
Li, J. & Pfeffer, S. R. Lysosomal membrane glycoproteins bind cholesterol and contribute to lysosomal cholesterol export. eLife. 5, e21635. https://doi.org/10.7554/eLife.21635 (2016).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Gu, J. et al. The role of lysosomal membrane proteins in glucose and lipid metabolism. FASEB J.35, e21848. https://doi.org/10.1096/fj.202002602R (2021).Article 
CAS 
PubMed 

Google Scholar 
Jenni-Eiermann, S. & Jenni, L. High plasma triglyceride levels in small birds during migratory flight: a new pathway for fuel supply during endurance locomotion at very high Mass-Specific Metabolic Rates? Physiol. Zool.65, 112–123. https://doi.org/10.1086/physzool.65.1.30158242 (1992).Article 
CAS 

Google Scholar 
Vock, R. et al. Design of the oxygen and substrate pathways: V. Structural basis of vascular substrate supply to muscle cells. J. Exp. Biol.199, 1675–1688. https://doi.org/10.1242/jeb.199.8.1675 (1996).Article 
CAS 
PubMed 

Google Scholar 
Wen, X., Jiao, L. & Tan, H. MAPK/ERK Pathway as a Central Regulator in Vertebrate Organ Regeneration. Int. J. Mol. Sci.23, 1464 (2022).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Meffert, M. K., Chang, J. M., Wiltgen, B. J., Fanselow, M. S. & Baltimore D. NF-κB functions in synaptic signaling and behavior. Nat. Neurosci.6, 1072–1078. https://doi.org/10.1038/nn1110 (2003).Article 
CAS 
PubMed 

Google Scholar 
Mattson, M. P. & Meffert, M. K. Roles for NF-κB in nerve cell survival, plasticity, and disease. Cell. Death Differ.13, 852–860. https://doi.org/10.1038/sj.cdd.4401837 (2006).Article 
CAS 
PubMed 

Google Scholar 
Voisin, S. et al. EPAS1 gene variants are associated with sprint/power athletic performance in two cohorts of European athletes. BMC Genom.15, 382. https://doi.org/10.1186/1471-2164-15-382 (2014).Article 

Google Scholar 
Bounas, A. et al. Adaptive regulation of stopover refueling during Bird Migration: insights from whole blood transcriptomics. Gen. Biol. Evol.15, evad061. https://doi.org/10.1093/gbe/evad061 (2023).Article 
CAS 

Google Scholar 
Wu, C. W., Biggar, K. K. & Storey, K. B. Biochemical adaptations of mammalian hibernation: exploring squirrels as a perspective model for naturally induced reversible insulin resistance. Braz. J. Med. Biol. Res.46, 1–13. https://doi.org/10.1590/1414-431×20122388 (2013).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Satoh, T. Bird evolution by insulin resistance. Trends Endocrinol. Metab.32, 803–813. https://doi.org/10.1016/j.tem.2021.07.007 (2021).Article 
CAS 
PubMed 

Google Scholar 
Gupta, N. J., Nanda, R. K., Das, S., Das, M. K. & Arya, R. Night migratory songbirds exhibit metabolic ability to Support High Aerobic Capacity during Migration. ACS Omega. 5, 28088–28095. https://doi.org/10.1021/acsomega.0c03691 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Sweazea, K. L., Tsosie, K. S., Beckman, E. J., Benham, P. M. & Witt, C. C. Seasonal and elevational variation in glucose and glycogen in two songbird species. Comp. Biochem. Physiol. A. 245, 110703. https://doi.org/10.1016/j.cbpa.2020.110703 (2020).Article 
CAS 

Google Scholar 
Price, E. R. et al. Migration- and exercise-induced changes to flight muscle size in migratory birds and association with IGF1 and myostatin mRNA expression. J. Exp. Biol.214, 2823–2831. https://doi.org/10.1242/jeb.057620 (2011).Article 
CAS 
PubMed 

Google Scholar 
Pradhan, D. S., Ma, C., Schlinger, B. A., Soma, K. K. & Ramenofsky, M. Preparing to migrate: expression of androgen signaling molecules and insulin-like growth factor-1 in skeletal muscles of Gambel’s white-crowned sparrows. J. Comp. Physiol. A. 205, 113–123. https://doi.org/10.1007/s00359-018-1308-7 (2019).Article 

Google Scholar 
Puigcerver, M. Contribución al conocimiento de la biología y ecoetología de la codorniz (Coturnix coturnix) phd thesis, University of Barcelona, (1991).Zduniak, P. & Yosef, R. Age and sex determine the phenology and biometrics of migratory common quail (Coturnix coturnix) at Eilat, Israel. Ornis Fennica. 85, 37–45 (2008).
Google Scholar 
Perennou, C. European Union Management Plan 2009–2011. Common Quail Coturnix coturnix (European Commission, 2009).Zuckerbrot, Y. D., Safriel, U. N. & Paz, U. Autumn migration of quail Coturnix coturnix at the north coast of the Sinai Peninsula. Ibis. 122, 1–14. https://doi.org/10.1111/j.1474-919X.1980.tb00867.x (1980).Article 

Google Scholar 
Franchini, P. et al. Animal tracking meets migration genomics: transcriptomic analysis of a partially migratory bird species. Mol. Ecol.26, 3204–3216. https://doi.org/10.1111/mec.14108 (2017).Article 
CAS 
PubMed 

Google Scholar 
Balthazart, J., Tlemçani, O. & Ball, G. F. Do sex differences in the brain explain sex differences in the Hormonal induction of Reproductive Behavior? What 25 years of Research on the Japanese quail tells us. Horm. Behav.30, 627–661. https://doi.org/10.1006/hbeh.1996.0066 (1996).Article 
CAS 
PubMed 

Google Scholar