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Genetic and ecological drivers of molt in a migratory bird

  • Stefansson, S. O., Björnsson, B. T., Ebbesson, L. O. E. & McCormick, S. D. Smoltification. In Fish Larval Physiology (eds Finn, R. N. & Kapoor, B. G.) 639–681 (CRC Press, 2020).

    Chapter 

    Google Scholar 

  • Kaleka, A. S., Kaur, N. & Bali, G. K. Larval development and molting. In Edible Insects (ed. Mikkola, H.) 17 (IntechOpen, 2019).

    Google Scholar 

  • Butler, L. K. & Rohwer, V. G. Feathers and molt. in Ornithology: Foundation, Analysis, and Application (eds Morrison, M. L. et al.) 242–270 (JHU Press, 2018).

    Google Scholar 

  • Swaddle, J. P., Witter, M. S., Cuthill, I. C., Budden, A. & McCowen, P. Plumage condition affects flight performance in common starlings: Implications for developmental homeostasis, abrasion and moult. J. Avian Biol. 27, 103–111 (1996).

    Article 

    Google Scholar 

  • Norris, D. R., Marra, P. P., Montgomerie, R., Kyser, T. K. & Ratcliffe, L. M. Reproductive effort, molting latitude, and feather color in a migratory songbird. Science 306, 2249–2250 (2004).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Delhey, K., Peters, A. & Kempenaers, B. Cosmetic coloration in birds: Occurrence, function, and evolution. Am. Nat. 169, S145–S158 (2007).

    Article 

    Google Scholar 

  • Tomotani, B. M. & Muijres, F. T. A songbird compensates for wing molt during escape flights by reducing the molt gap and increasing angle of attack. J. Exp. Biol. 222, 195396 (2019).

    Article 

    Google Scholar 

  • Galván, I., Negro, J. J., Rodriguez, A. & Carrascal, L. M. On showy dwarfs and sober giants: Body size as a constraint for the evolution of bird plumage colouration. Acta Ornithol. 48, 65–80 (2013).

    Article 

    Google Scholar 

  • Speakman, J. R. & Król, E. Maximal heat dissipation capacity and hyperthermia risk: Neglected key factors in the ecology of endotherms. J. Anim. Ecol. 79, 726–746 (2010).

    Google Scholar 

  • Wolf, B. O. & Walsberg, G. E. The role of the plumage in heat transfer processes of birds. Am. Zool. 40, 575–584 (2000).

    Google Scholar 

  • Berthold, P. & Querner, U. Genetic basis of moult, wing length, and body weight in a migratory bird species, Sylvia atricapilla. Experientia 38, 801–802 (1982).

    Article 

    Google Scholar 

  • Gwinner, E., Neusser, V., Engl, D., Schmidl, D. & Bals, L. Haltung, Zucht und Eiaufzucht afrikanischer und europäischer Schwarzkehlchen Saxicola torquata. Gefied. Welt 111, 118–120 (1987).

    Google Scholar 

  • Berthold, P. & Querner, U. Microevolutionary aspects of bird migration based on experimental results. Isr. J. Ecol. Evol. 41, 377–385 (1995).

    Google Scholar 

  • Helm, B. & Gwinner, E. Timing of postjuvenal molt in African (Saxicola torquata axillaris) and European (Saxicola torquata rubicola) stonechats: Effects of genetic and environmental factors. Auk 116, 589–603 (1999).

    Article 

    Google Scholar 

  • Helm, B. & Gwinner, E. Timing of molt as a buffer in the avian annual cycle. Acta Zool. Sin. 52, 703–706 (2006).

    Google Scholar 

  • Rohwer, S., Ricklefs, R. E., Rohwer, V. G. & Copple, M. M. Allometry of the duration of flight feather molt in birds. PLoS Biol. 7, e1000132 (2009).

    Article 

    Google Scholar 

  • Jenni, L. & Winkler, R. The Biology of Moult in Birds (Bloomsbury Publishing, 2020).

    Google Scholar 

  • Tonra, C. M. & Reudink, M. W. Expanding the traditional definition of molt-migration. Auk Ornithol. Adv. 135, 1123–1132 (2018).

    Google Scholar 

  • Rohwer, S., Butler, L. K., Froehlich, D. R., Greenberg, R. & Marra, P. P. Ecology and demography of east–west differences in molt scheduling of Neotropical migrant passerines. Birds Two Worlds Ecol. Evol. Migr. (R. Greenb. PP Marra, Eds.). Johns Hopkins Univ. Press. Balt. Maryl., 87–105 (2005).

  • Bensch, S., Åkesson, S. & Irwin, D. E. The use of AFLP to find an informative SNP: Genetic differences across a migratory divide in willow warblers. Mol. Ecol. 11, 2359–2366 (2002).

    Article 
    CAS 

    Google Scholar 

  • Ruegg, K. Genetic, morphological, and ecological characterization of a hybrid zone that spans a migratory divide. Evol. Int. J. Org. Evol. 62, 452–466 (2008).

    Article 

    Google Scholar 

  • Delmore, K. E., Fox, J. W. & Irwin, D. E. Dramatic intraspecific differences in migratory routes, stopover sites and wintering areas, revealed using light-level geolocators. Proc. R. Soc. B Biol. Sci. 279, 4582–4589 (2012).

    Article 

    Google Scholar 

  • Delmore, K. E. et al. Individual variability and versatility in an eco-evolutionary model of avian migration. Proc. R. Soc. B 287, 20201339 (2020).

    Article 

    Google Scholar 

  • Procházka, P. et al. Across a migratory divide: divergent migration directions and non-breeding grounds of Eurasian reed warblers revealed by geolocators and stable isotopes. J. Avian Biol. 49, 012516 (2018).

    Article 

    Google Scholar 

  • Bensch, S., Grahn, M., Müller, N., Gay, L. & Åkesson, S. Genetic, morphological, and feather isotope variation of migratory willow warblers show gradual divergence in a ring. Mol. Ecol. 18, 3087–3096 (2009).

    Article 

    Google Scholar 

  • Rohwer, S. & Irwin, D. E. Molt, orientation, and avian speciation. Auk 128, 419–425 (2011).

    Article 

    Google Scholar 

  • Pageau, C., Sonnleitner, J., Tonra, C. M., Shaikh, M. & Reudink, M. W. Evolution of winter molting strategies in European and North American migratory passerines. Ecol. Evol. 11, 13247–13258 (2021).

    Article 

    Google Scholar 

  • Butler, L. K., Rohwer, S. & Rogers, M. Prebasic molt and molt-related movements in Ash-throated Flycatchers. Condor 108, 647–660 (2006).

    Article 

    Google Scholar 

  • Barry, J. H., Butler, L. K., Rohwer, S. & Rohwer, V. G. Documenting molt-migration in Western Kingbird (Tyrannus verticalis) using two measures of collecting effort. Auk 126, 260–267 (2009).

    Article 

    Google Scholar 

  • Hobson, K. A. & Wassenaar, L. I. Linking breeding and wintering grounds of neotropical migrant songbirds using stable hydrogen isotopic analysis of feathers. Oecologia 109, 142–148 (1996).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Hobson, K. A. & Wassenaar, L. I. Tracking Animal Migration with Stable Isotopes (Academic Press, 2018).

    Google Scholar 

  • Rubenstein, D. R. & Hobson, K. A. From birds to butterflies: Animal movement patterns and stable isotopes. Trends Ecol. Evol. 19, 256–263 (2004).

    Article 

    Google Scholar 

  • Bearhop, S. et al. Assortative mating as a mechanism for rapid evolution of a migratory divide. Science 310, 502–504 (2005).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Eppig, J. T. et al. The mouse genome database (MGD): Comprehensive resource for genetics and genomics of the laboratory mouse. Nucleic Acids Res. 40, D881–D886 (2012).

    Article 
    CAS 

    Google Scholar 

  • Contina, A., Bridge, E. S. & Kelly, J. F. Exploring novel candidate genes from the mouse genome informatics database: Potential implications for avian migration research. Integr. Zool. 11, 240 (2016).

    Article 

    Google Scholar 

  • Yang, J. et al. Common SNPs explain a large proportion of the heritability for human height. Nat. Genet. 42, 565–569 (2010).

    Article 
    CAS 

    Google Scholar 

  • Thompson, C. W. Is the Painted Bunting actually two species? Problems determining species limits between allopatric populations. Condor 93, 987–1000 (1991).

    Article 

    Google Scholar 

  • Contina, A., Bridge, E. S., Seavy, N. E., Duckles, J. M. & Kelly, J. F. Using geologgers to investigate bimodal isotope patterns in Painted Buntings (Passerina ciris). Auk 130, 265 (2013).

    Article 

    Google Scholar 

  • Besozzi, E., Chew, B., Allen, D. C. & Contina, A. Stable isotope analysis of an aberrant Painted Bunting (Passerina ciris) feather suggests post-molt movements. Wilson J. Ornithol. 133, 151 (2021).

    Article 

    Google Scholar 

  • Sharp, A. et al. Spatial and Temporal Scale-Dependence of the Strength of Migratory Connectivity in a North American Passerine. https://assets.researchsquare.com/files/rs-1483049/v1/72236b63-952d-4870-89e7-461056b8625b.pdf?c=1648893558 (2022).

  • Pyle, P. et al. Temporal, spatial, and annual variation in the occurrence of molt-migrant passerines in the Mexican monsoon region. Condor 111, 583–590 (2009).

    Article 

    Google Scholar 

  • Bridge, E. S., Fudickar, A. M., Kelly, J. F., Contina, A. & Rohwer, S. Causes of bimodal stable isotope signatures in the feathers of a molt-migrant songbird. Can. J. Zool. 89, 951 (2011).

    Article 
    CAS 

    Google Scholar 

  • Seutin, G., White, B. N. & Boag, P. T. Preservation of avian blood and tissue samples for DNA analyses. Can. J. Zool. 69, 82–90 (1991).

    Article 
    CAS 

    Google Scholar 

  • Ali, O. A. et al. RAD capture rapture: Flexible and efficient sequence-based genotyping. Genetics 202, 389–400 (2016).

    Article 
    CAS 

    Google Scholar 

  • Contina, A. et al. Characterization of SNP markers for the Painted Bunting (Passerina ciris) and their relevance in population differentiation and genome evolution studies. Conserv. Genet. Resour. 11, 5–10 (2019).

    Article 
    ADS 

    Google Scholar 

  • Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A. & Cresko, W. A. Stacks: An analysis tool set for population genomics. Mol. Ecol. 22, 3124–3140 (2013).

    Article 

    Google Scholar 

  • Parker, P., Li, B., Li, H. & Wang, J. The genome of Darwin’s Finch (Geospiza fortis). Gigascience 10, 100040 (2012).

    Google Scholar 

  • Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).

    Article 
    CAS 

    Google Scholar 

  • Van der Auwera, G. A. et al. From FastQ data to high-confidence variant calls: The genome analysis toolkit best practices pipeline. Curr. Protoc. Bioinform. 43, 1–33 (2013).

    Google Scholar 

  • McKenna, A. et al. The genome analysis toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).

    Article 
    CAS 

    Google Scholar 

  • Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011).

    Article 
    CAS 

    Google Scholar 

  • Anderson, E. genoscapeRtools: Tools for Building Migratory Bird Genoscapes (2019).

  • Purcell, S. et al. PLINK: A tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007).

    Article 
    CAS 

    Google Scholar 

  • Alexander, D. H., Novembre, J. & Lange, K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655–1664 (2009).

    Article 
    CAS 

    Google Scholar 

  • Alexander, D. H. & Lange, K. Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC Bioinform. 12, 246 (2011).

    Article 

    Google Scholar 

  • Francis, R. M. pophelper: An R package and web app to analyse and visualize population structure. Mol. Ecol. Resour. 17, 27–32 (2017).

    Article 
    CAS 

    Google Scholar 

  • Chew, B., Kelly, J. & Contina, A. Stable isotopes in avian research: a step by step protocol to feather sample preparation for stable isotope analysis of carbon (δ13C), nitrogen (δ15N), and hydrogen (δ2H). Version 1.1. https://doi.org/10.17504/protocols.io.z2uf8ew (2019).

  • Wassenaar, L. I. & Hobson, K. A. Comparative equilibration and online technique for determination of non-exchangeable hydrogen of keratins for use in animal migration studies. Isotopes Environ. Health Stud. 39(3), 211–217 (2003).

    Article 
    CAS 

    Google Scholar 

  • Bowen, G. J., Wassenaar, L. I. & Hobson, K. A. Global application of stable hydrogen and oxygen isotopes to wildlife forensics. Oecologia 143, 337–348 (2005).

    Article 
    ADS 

    Google Scholar 

  • R Core Team: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2021).

  • Wassenaar, L. I. & Hobson, K. A. Stable-hydrogen isotope heterogeneity in keratinous materials: Mass spectrometry and migratory wildlife tissue subsampling strategies. Rapid Commun. Mass Spectrom. 20, 2505–2510 (2006).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Zhou, X., Carbonetto, P. & Stephens, M. Polygenic modeling with Bayesian sparse linear mixed models. PLoS Genet. 9, e1003264 (2013).

    Article 
    CAS 

    Google Scholar 

  • Guan, Y. & Stephens, M. Bayesian variable selection regression for genome-wide association studies and other large-scale problems. Ann. Appl. Stat. 5, 455 (2011).

    Article 
    MathSciNet 
    MATH 

    Google Scholar 

  • Marchini, J., Cardon, L. R., Phillips, M. S. & Donnelly, P. The effects of human population structure on large genetic association studies. Nat. Genet. 36, 512–517 (2004).

    Article 
    CAS 

    Google Scholar 

  • Browning, S. R. & Browning, B. L. Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am. J. Hum. Genet. 81, 1084–1097 (2007).

    Article 
    CAS 

    Google Scholar 

  • Chaves, J. A. et al. Genomic variation at the tips of the adaptive radiation of Darwin’s finches. Mol. Ecol. 25, 5282–5295 (2016).

    Article 
    CAS 

    Google Scholar 

  • Zhang, Y.-W. et al. mrMLM v4.0.2: An R platform for multi-locus genome-wide association studies. Genom. Proteom. Bioinform. 18, 481–487 (2020).

    Article 

    Google Scholar 

  • Grabherr, M. G. et al. Genome-wide synteny through highly sensitive sequence alignment: Satsuma. Bioinformatics 26, 1145–1151 (2010).

    Article 
    CAS 

    Google Scholar 

  • Quinlan, A. R. & Hall, I. M. BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).

    Article 
    CAS 

    Google Scholar 

  • Ellis, N., Smith, S. J. & Pitcher, C. R. Gradient forests: Calculating importance gradients on physical predictors. Ecology 93, 156–168 (2012).

    Article 

    Google Scholar 

  • Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).

    Article 

    Google Scholar 

  • Anderson, E. C. snps2assays: Prepare SNP Assay Orders from ddRAD or RAD Loci (2015).

  • Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

    Article 
    CAS 

    Google Scholar 

  • Patterson, N., Price, A. L. & Reich, D. Population structure and eigenanalysis. PLoS Genet. 2, e190 (2006).

    Article 

    Google Scholar 

  • Price, A. L. et al. Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet. 38, 904–909 (2006).

    Article 
    CAS 

    Google Scholar 

  • Ruegg, K. et al. Ecological genomics predicts climate vulnerability in an endangered southwestern songbird. Ecol. Lett. 21, 1085–1096 (2018).

    Article 

    Google Scholar 

  • Bay, R. A. et al. Genomic signals of selection predict climate-driven population declines in a migratory bird. Science 359, 83–86 (2018).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Hedenström, A. Adaptations to migration in birds: Behavioural strategies, morphology and scaling effects. Philos. Trans. R. Soc. B Biol. Sci. 363, 287–299 (2008).

    Article 

    Google Scholar 

  • Buehler, D. M. & Piersma, T. Travelling on a budget: Predictions and ecological evidence for bottlenecks in the annual cycle of long-distance migrants. Philos. Trans. R. Soc. B Biol. Sci. 363, 247–266 (2008).

    Article 

    Google Scholar 

  • Schieltz, P. C. & Murphy, M. E. The contribution of insulation changes to the energy cost of avian molt. Can. J. Zool. 75, 396–400 (1997).

    Article 

    Google Scholar 

  • Carling, M. D. & Thomassen, H. A. The role of environmental heterogeneity in maintaining reproductive isolation between hybridizing Passerina (Aves: Cardinalidae) buntings. Int. J. Ecol. 2012, 1–11 (2012).

    Article 

    Google Scholar 

  • Irwin, D. E. Incipient ring speciation revealed by a migratory divide. Mol. Ecol. 18, 2923–2925 (2009).

    Article 

    Google Scholar 

  • Thomas, D. W., Blondel, J., Perret, P., Lambrechts, M. M. & Speakman, J. R. Energetic and fitness costs of mismatching resource supply and demand in seasonally breeding birds. Science 291, 2598–2600 (2001).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Rohwer, V. G., Rohwer, S. & Ortiz-Ramirez, M. F. Molt biology of resident and migrant birds of the monsoon region of west Mexico. Ornitol. Neotrop. 20, 565–584 (2009).

    Google Scholar 

  • Bensch, S., Andersson, T. & Åkesson, S. Morphological and molecular variation across a migratory divide in willow warblers, Phylloscopus trochilus. Evolution 53, 1925–1935 (1999).

    Article 

    Google Scholar 

  • Turbek, S. P., Scordato, E. S. C. & Safran, R. J. The role of seasonal migration in population divergence and reproductive isolation. Trends Ecol. Evol. 33, 164–175 (2018).

    Article 

    Google Scholar 

  • Scordato, E. S. C. et al. Migratory divides coincide with reproductive barriers across replicated avian hybrid zones above the Tibetan Plateau. Ecol. Lett. 23, 231–241 (2020).

    Article 

    Google Scholar 

  • Battey, C. J. et al. A migratory divide in the Painted Bunting (Passerina ciris). Am. Nat. 191, 259–268 (2018).

    Article 
    CAS 

    Google Scholar 

  • Contina, A. et al. Genetic structure of the Painted Bunting and its implications for conservation of migratory populations. Ibis 161, 372 (2019).

    Article 

    Google Scholar 

  • Butler, L. K. The grass is always greener: Do monsoon rains matter for molt of the Vermilion Flycatcher (Pyrocephalus rubinus)? Auk 130, 297–307 (2013).

    Article 

    Google Scholar 

  • Turbek, S. P. et al. A migratory divide spanning two continents is associated with genomic and ecological divergence. Evolution 76, 722 (2022).

    Article 

    Google Scholar 

  • Dietz, M. W., Daan, S. & Masman, D. Energy requirements for molt in the kestrel Falco tinnunculus. Physiol. Zool. 65, 1217–1235 (1992).

    Article 

    Google Scholar 

  • Vézina, F., Gustowska, A., Jalvingh, K. M., Chastel, O. & Piersma, T. Hormonal correlates and thermoregulatory consequences of molting on metabolic rate in a northerly wintering shorebird. Physiol. Biochem. Zool. 82, 129–142 (2009).

    Article 

    Google Scholar 

  • Bazzi, G. et al. 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 (2017).

    CAS 

    Google Scholar 

  • Busby, L. et al. Sonic hedgehog specifies flight feather positional information in avian wings. Development 147, 188821 (2020).

    Article 

    Google Scholar 

  • Eichberger, T. et al. GLI2-specific transcriptional activation of the bone morphogenetic protein/Activin antagonist Follistatin in human epidermal cells. J. Biol. Chem. 283, 12426–12437 (2008).

    Article 
    CAS 

    Google Scholar 

  • Matzuk, M. M. et al. Multiple defects and perinatal death in mice deficient in follistatin. Nature 374, 360–363 (1995).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Patel, K., Makarenkova, H. & Jung, H.-S. 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 (1999).

    Article 
    CAS 

    Google Scholar 

  • Nakamura, M. et al. Control of pelage hair follicle development and cycling by complex interactions between follistatin and activin. FASEB J. 17, 1–22 (2003).

    Article 
    MathSciNet 

    Google Scholar 

  • Pays, L., Charvet, I., Hemming, F. J. & Saxod, R. Close link between cutaneous nerve pattern development and feather morphogenesis demonstrated by experimental production of neo-apteria and ectopic feathers: Implication of chondroitin sulphate proteoglycans and other matrix molecules. Anat. Embryol. 195, 457–466 (1997).

    Article 
    CAS 

    Google Scholar 

  • Pyle, P., Saracco, J. F. & DeSante, D. F. Evidence of widespread movements from breeding to molting grounds by North American landbirds. Auk Ornithol. Adv. 135, 506–520 (2018).

    Google Scholar 

  • De Mita, S. et al. Detecting selection along environmental gradients: Analysis of eight methods and their effectiveness for outbreeding and selfing populations. Mol. Ecol. 22, 1383–1399 (2013).

    Article 

    Google Scholar 

  • Lotterhos, K. E. & Whitlock, M. C. Evaluation of demographic history and neutral parameterization on the performance of FST outlier tests. Mol. Ecol. 23, 2178–2192 (2014).

    Article 

    Google Scholar 

  • Frichot, E., Schoville, S. D., de Villemereuil, P., Gaggiotti, O. E. & François, O. Detecting adaptive evolution based on association with ecological gradients: Orientation matters!. Heredity (Edinb.) 115, 22–28 (2015).

    Article 
    CAS 

    Google Scholar 

  • Trivedi, A. K. et al. Temperature alters the hypothalamic transcription of photoperiod responsive genes in induction of seasonal response in migratory redheaded buntings. Mol. Cell. Endocrinol. 493, 110454 (2019).

    Article 
    CAS 

    Google Scholar 


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