{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,15]],"date-time":"2026-10-15T05:28:37Z","timestamp":1792042117025,"version":"4.4.0"},"reference-count":74,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,9,18]],"date-time":"2021-09-18T00:00:00Z","timestamp":1631923200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,9,18]],"date-time":"2021-09-18T00:00:00Z","timestamp":1631923200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100003130","name":"Fonds Wetenschappelijk Onderzoek","doi-asserted-by":"publisher","award":["G078814N"],"award-info":[{"award-number":["G078814N"]}],"id":[{"id":"10.13039\/501100003130","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003130","name":"Fonds Wetenschappelijk Onderzoek","doi-asserted-by":"publisher","award":["SBO151086"],"award-info":[{"award-number":["SBO151086"]}],"id":[{"id":"10.13039\/501100003130","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Ecol Evo"],"abstract":"<jats:title>Abstract<\/jats:title><jats:sec>\n                <jats:title>Background<\/jats:title>\n                <jats:p>Approximately 1000 protein encoding genes common for vertebrates are still unannotated in avian genomes. Are these genes evolutionary lost or are they not yet found for technical reasons? Using genome landscapes as a tool to visualize large-scale regional effects of genome evolution, we reexamined this question.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>On basis of gene annotation in non-avian vertebrate genomes, we established a list of 15,135 common vertebrate genes. Of these, 1026 were not found in any of eight examined bird genomes. Visualizing regional genome effects by our sliding window approach showed that the majority of these \"missing\" genes can be clustered to 14 regions of the human reference genome. In these clusters, an additional 1517 genes (often gene fragments) were underrepresented in bird genomes. The clusters of \u201cmissing\u201d genes coincided with regions of very high GC content, particularly in avian genomes, making them \u201chidden\u201d because of incomplete sequencing. Moreover, proteins encoded by genes in these sequencing refractory regions showed signs of accelerated protein evolution. As a proof of principle for this idea we experimentally characterized the mRNA and protein products of four \"hidden\" bird genes that are crucial for energy homeostasis in skeletal muscle: <jats:italic>ALDOA<\/jats:italic>, <jats:italic>ENO3<\/jats:italic>, <jats:italic>PYGM<\/jats:italic> and <jats:italic>SLC2A4<\/jats:italic>.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Conclusions<\/jats:title>\n                <jats:p>A least part of the \u201cmissing\u201d genes in bird genomes can be attributed to an artifact caused by the difficulty to sequence regions with extreme GC% (\u201chidden\u201d genes). Biologically, these \u201chidden\u201d genes are of interest as they encode proteins that evolve more rapidly than the genome wide average. Finally we show that four of these \u201chidden\u201d genes encode key proteins for energy metabolism in flight muscle.<\/jats:p>\n              <\/jats:sec>","DOI":"10.1186\/s12862-021-01905-7","type":"journal-article","created":{"date-parts":[[2021,9,18]],"date-time":"2021-09-18T10:03:31Z","timestamp":1631959411000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":20,"title":["Sequencing refractory regions in bird genomes are hotspots for accelerated protein evolution"],"prefix":"10.1186","volume":"21","author":[{"given":"R.","family":"Huttener","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"L.","family":"Thorrez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"T. In\u2019t","family":"Veld","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M.","family":"Granvik","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"L.","family":"Van Lommel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"E.","family":"Waelkens","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"R.","family":"Derua","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"K.","family":"Lemaire","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"L.","family":"Goyvaerts","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"S.","family":"De Coster","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J.","family":"Buyse","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3225-6695","authenticated-orcid":false,"given":"F.","family":"Schuit","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,9,18]]},"reference":[{"key":"1905_CR1","doi-asserted-by":"publisher","first-page":"807","DOI":"10.1038\/nature01420","volume":"421","author":"Z Zhou","year":"2003","unstructured":"Zhou Z, Barrett PM, Hilton J. An exceptionally preserved Lower Cretaceous ecosystem. Nature. 2003;421:807\u201314.","journal-title":"Nature"},{"key":"1905_CR2","doi-asserted-by":"publisher","first-page":"R888","DOI":"10.1016\/j.cub.2015.08.003","volume":"25","author":"SL Brusatte","year":"2015","unstructured":"Brusatte SL, O\u2019Connor JK, Jarvis ED. The origin and diversification of birds. Curr Biol. 2015;25:R888\u201398.","journal-title":"Curr Biol"},{"key":"1905_CR3","doi-asserted-by":"publisher","first-page":"1311","DOI":"10.1126\/science.1251385","volume":"346","author":"G Zhang","year":"2014","unstructured":"Zhang G, Li C, Li Q, Li B, Larkin DM, Lee C, et al. Comparative genomics reveals insights into avian genome evolution and adaptation. Science. 2014;346:1311\u201320.","journal-title":"Science"},{"key":"1905_CR4","doi-asserted-by":"publisher","first-page":"1320","DOI":"10.1126\/science.1253451","volume":"346","author":"ED Jarvis","year":"2014","unstructured":"Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P, Li C, et al. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science. 2014;346:1320\u201331.","journal-title":"Science"},{"key":"1905_CR5","first-page":"155","volume":"125","author":"KJ Carpenter","year":"1995","unstructured":"Carpenter KJ, Sutherland B. Eijkman\u2019s contribution to the discovery of vitamins. J Nutr. 1995;125:155\u201363.","journal-title":"J Nutr"},{"key":"1905_CR6","doi-asserted-by":"publisher","first-page":"695","DOI":"10.1038\/nature03154","volume":"432","author":"LW Hillier","year":"2004","unstructured":"Hillier LW, Miller W, Birney E, Warren W, Hardison RC, Ponting CP, et al. Sequencing and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature. 2004;432:695\u2013716.","journal-title":"Nature"},{"key":"1905_CR7","doi-asserted-by":"publisher","first-page":"1057","DOI":"10.1093\/ps\/86.6.1057","volume":"86","author":"CG Scanes","year":"2007","unstructured":"Scanes CG. The global importance of poultry. Poult Sci. 2007;86:1057\u20138.","journal-title":"Poult Sci"},{"key":"1905_CR8","doi-asserted-by":"crossref","unstructured":"Warren WC, Hillier LW, Tomlinson C, Minx P, Kremitzki M, Graves T, et al. A new chicken genome assembly provides insight into avian genome structure. G3 (Bethesda). 2017;7:109\u201317.","DOI":"10.1534\/g3.116.035923"},{"key":"1905_CR9","doi-asserted-by":"publisher","first-page":"252","DOI":"10.1038\/s41586-020-2873-9","volume":"587","author":"S Feng","year":"2020","unstructured":"Feng S, Stiller J, Deng Y, Armstrong J, Fang Q, Reeve AH, et al. Dense sampling of bird diversity increases power of comparative genomics. Nature. 2020;587:252\u20137.","journal-title":"Nature"},{"key":"1905_CR10","doi-asserted-by":"publisher","first-page":"565","DOI":"10.1186\/s13059-014-0565-1","volume":"15","author":"PV Lovell","year":"2014","unstructured":"Lovell PV, Wirthlin M, Wilhelm L, Minx P, Lazar NH, Carbone L, et al. Conserved syntenic clusters of protein coding genes are missing in birds. Genome Biol. 2014;15:565.","journal-title":"Genome Biol"},{"key":"1905_CR11","doi-asserted-by":"publisher","first-page":"498","DOI":"10.1038\/nature12111","volume":"496","author":"K Howe","year":"2013","unstructured":"Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, et al. The zebrafish reference genome sequence and its relationship to the human genome. Nature. 2013;496:498\u2013503.","journal-title":"Nature"},{"key":"1905_CR12","doi-asserted-by":"publisher","first-page":"164","DOI":"10.1186\/s13059-015-0724-z","volume":"16","author":"T Hron","year":"2015","unstructured":"Hron T, Pajer P, Pa\u010des J, Bart\u016fn\u011bk P, Elleder D. Hidden genes in birds. Genome Biol. 2015;16:164.","journal-title":"Genome Biol"},{"key":"1905_CR13","doi-asserted-by":"publisher","first-page":"R51","DOI":"10.1186\/gb-2013-14-5-r51","volume":"14","author":"MG Ross","year":"2013","unstructured":"Ross MG, Russ C, Costello M, Hollinger A, Lennon NJ, Hegarty R, et al. Characterizing and measuring bias in sequence data. Genome Biol. 2013;14:R51.","journal-title":"Genome Biol"},{"key":"1905_CR14","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/srep00055","volume":"1","author":"W Wang","year":"2011","unstructured":"Wang W, Wei Z, Lam T-W, Wang J. Next generation sequencing has lower sequence coverage and poorer SNP-detection capability in the regulatory regions. Sci Rep. 2011;1:1\u20137.","journal-title":"Sci Rep"},{"key":"1905_CR15","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pone.0094650","volume":"9","author":"S Thomas","year":"2014","unstructured":"Thomas S, Underwood JG, Tseng E, Holloway AK. Long-read sequencing of chicken transcripts and identification of new transcript isoforms. PLoS ONE. 2014;9:1\u20136.","journal-title":"PLoS ONE"},{"key":"1905_CR16","doi-asserted-by":"crossref","unstructured":"Botero-Castro F, Figuet E, Tilak M, Nabholz B, Galtier N. Avian genomes revisited: hidden genes uncovered and the rates vs. traits paradox in birds. Mol Biol Evol. 2017;34(March):3123\u201331.","DOI":"10.1093\/molbev\/msx236"},{"key":"1905_CR17","doi-asserted-by":"crossref","unstructured":"Yin ZT, Zhu F, Lin F Bin, Jia T, Wang Z, Sun DT, et al. Revisiting avian \u201cmissing\u201d genes from de novo assembled transcripts. BMC Genomics. 2019;20:1\u201310.","DOI":"10.1186\/s12864-018-5407-1"},{"key":"1905_CR18","doi-asserted-by":"publisher","first-page":"425","DOI":"10.1038\/372425a0","volume":"372","author":"Y Zhang","year":"1994","unstructured":"Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM. Positional cloning of the mouse obese gene and its human homologue. Nature. 1994;372:425\u201332.","journal-title":"Nature"},{"key":"1905_CR19","doi-asserted-by":"publisher","first-page":"543","DOI":"10.1126\/science.7624777","volume":"269","author":"JL Halaas","year":"1995","unstructured":"Halaas JL, Gajiwala KS, Maffei M, Cohen SL, Chait BT, Rabinowitz D, et al. Weight-reducing effects of the plasma protein encoded by the obese gene. Science. 1995;269:543\u20136.","journal-title":"Science"},{"key":"1905_CR20","doi-asserted-by":"publisher","first-page":"737","DOI":"10.1210\/en.2015-1634","volume":"157","author":"E Seroussi","year":"2016","unstructured":"Seroussi E, Cinnamon Y, Yosefi S, Genin O, Smith JG, Rafati N, et al. Identification of the long-sought leptin in chicken and duck: expression pattern of the highly GC-Rich avian leptin fits an autocrine\/paracrine rather than endocrine function. Endocrinology. 2016;157:737\u201351.","journal-title":"Endocrinology"},{"key":"1905_CR21","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1186\/s12863-017-0543-1","volume":"18","author":"E Seroussi","year":"2017","unstructured":"Seroussi E, Pitel F, Leroux S, Morisson M, Bornel\u00f6v S, Miyara S, et al. Mapping of leptin and its syntenic genes to chicken chromosome 1p. BMC Genet. 2017;18:77.","journal-title":"BMC Genet"},{"key":"1905_CR22","doi-asserted-by":"publisher","first-page":"819","DOI":"10.1016\/j.tem.2019.07.007","volume":"30","author":"M Friedman-Einat","year":"2019","unstructured":"Friedman-Einat M, Seroussi E. Avian leptin: bird\u2019s-eye view of the evolution of vertebrate energy-balance control. Trends Endocrinol Metab. 2019;30:819\u201332.","journal-title":"Trends Endocrinol Metab"},{"key":"1905_CR23","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1016\/j.mam.2012.07.001","volume":"34","author":"M Mueckler","year":"2013","unstructured":"Mueckler M, Thorens B. The SLC2 (GLUT) family of membrane transporters. Mol Aspects Med. 2013;34:121\u201338.","journal-title":"Mol Aspects Med"},{"key":"1905_CR24","first-page":"E309","volume":"274","author":"J Dupont","year":"1998","unstructured":"Dupont J, Derouet M, Simon J, Taouis M. Nutritional state regulates insulin receptor and IRS-1 phosphorylation and expression in chicken. Am J Physiol. 1998;274:E309\u201316.","journal-title":"Am J Physiol"},{"key":"1905_CR25","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.cbpb.2008.05.007","volume":"151","author":"EJ Braun","year":"2008","unstructured":"Braun EJ, Sweazea KL. Glucose regulation in birds. Comp Biochem Physiol B. 2008;151:1\u20139.","journal-title":"Comp Biochem Physiol B"},{"key":"1905_CR26","doi-asserted-by":"crossref","unstructured":"Huttener R, Thorrez L, In\u2019t Veld T, Granvik M, Snoeck L, Van Lommel L, et al. GC content of vertebrate exome landscapes reveal areas of accelerated protein evolution. BMC Evol Biol. 2019;19:144.","DOI":"10.1186\/s12862-019-1469-1"},{"key":"1905_CR27","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1186\/s13059-015-0725-y","volume":"16","author":"PV Lovell","year":"2015","unstructured":"Lovell PV, Wirthlin M, Carbone L, Warren WC, Mello CV, et al. Response to Hron et al. Genome Biol. 2015;16:165.","journal-title":"Genome Biol"},{"key":"1905_CR28","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s13059-017-1231-1","volume":"18","author":"S Bornel\u00f6v","year":"2017","unstructured":"Bornel\u00f6v S, Seroussi E, Yosefi S, Pendavis K, Burgess SC, Grabherr M, et al. Correspondence on Lovell et al.: identification of chicken genes previously assumed to be evolutionarily lost. Genome Biol. 2017;18:1\u20134.","journal-title":"Genome Biol"},{"key":"1905_CR29","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1093\/nar\/gks001","volume":"40","author":"Y Benjamini","year":"2012","unstructured":"Benjamini Y, Speed TP. Summarizing and correcting the GC content bias in high-throughput sequencing. Nucleic Acids Res. 2012;40:1\u201314.","journal-title":"Nucleic Acids Res"},{"key":"1905_CR30","doi-asserted-by":"publisher","first-page":"2779","DOI":"10.1093\/nar\/15.6.2779","volume":"15","author":"C Carlberg","year":"1987","unstructured":"Carlberg C, Quaas R, Hahn U, Wittig B. Sequencing refractory GC rich regions in plasmid DNA. Nucleic Acids Res. 1987;15:2779.","journal-title":"Nucleic Acids Res"},{"key":"1905_CR31","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1042\/bj3500099","volume":"350","author":"AM Shewan","year":"2000","unstructured":"Shewan AM, Marsh BJ, Melvin DR, Martin S, Gould GW, James DE. The cytosolic C-terminus of the glucose transporter GLUT4 contains an acidic cluster endosomal targeting motif distal to the dileucine signal. Biochem J. 2000;350:99\u2013107.","journal-title":"Biochem J"},{"issue":"Pt 10","key":"1905_CR32","doi-asserted-by":"publisher","first-page":"1705","DOI":"10.1242\/jcs.113.10.1705","volume":"113","author":"S Martinez-Arca","year":"2000","unstructured":"Martinez-Arca S, Lalioti VS, Sandoval IV. Intracellular targeting and retention of the glucose transporter GLUT4 by the perinuclear storage compartment involves distinct carboxyl-tail motifs. J Cell Sci. 2000;113(Pt 10):1705\u201315.","journal-title":"J Cell Sci"},{"key":"1905_CR33","doi-asserted-by":"crossref","unstructured":"Melvin DR, Marsh BJ, Walmsley AR, James DE, Gould GW. Analysis of amino and carboxy terminal glut-4 targeting motifs in 3T3-L1 adipocytes using an endosomal ablation technique. Biochemistry. 1999;38:1456\u201362.","DOI":"10.1021\/bi980988y"},{"key":"1905_CR34","doi-asserted-by":"crossref","unstructured":"Blot V, Mcgraw TE. Molecular mechanisms controlling GLUT4 intracellular retention. Mol Biol Cell. 2008;19(August):3477\u201387.","DOI":"10.1091\/mbc.e08-03-0236"},{"key":"1905_CR35","doi-asserted-by":"crossref","unstructured":"Denyer MP, Pinheiro DY, Garden OA, Shepherd AJ. Missed, not missing: phylogenomic evidence for the existence of avian FoxP3. PLoS ONE. 2016;11:e0150988.","DOI":"10.1371\/journal.pone.0150988"},{"key":"1905_CR36","doi-asserted-by":"crossref","unstructured":"Shin SC, Ahn DH, Kim SJ, Lee H, Oh T-J, Lee JE, et al. Advantages of single-molecule real-time sequencing in high-GC content genomes. PLoS ONE. 2013;8:e68824.","DOI":"10.1371\/journal.pone.0068824"},{"key":"1905_CR37","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1093\/gigascience\/gix085","volume":"6","author":"J Korlach","year":"2017","unstructured":"Korlach J, Gedman G, Kingan SB, Chin CS, Howard JT, Audet JN, et al. De novo PacBio long-read and phased avian genome assemblies correct and add to reference genes generated with intermediate and short reads. Gigascience. 2017;6:1\u201316.","journal-title":"Gigascience"},{"key":"1905_CR38","doi-asserted-by":"publisher","first-page":"96","DOI":"10.1046\/j.1365-2052.2000.00565.x","volume":"31","author":"J Smith","year":"2000","unstructured":"Smith J, Bruley CK, Paton IR, Dunn I, Jones CT, Windsor D, et al. Differences in gene density on chicken macrochromosomes and microchromosomes. Anim Genet. 2000;31:96\u2013103.","journal-title":"Anim Genet"},{"key":"1905_CR39","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1159\/000063018","volume":"96","author":"DW Burt","year":"2002","unstructured":"Burt DW. Origin and evolution of avian microchromosomes. Cytogenet Genome Res. 2002;96:97\u2013112.","journal-title":"Cytogenet Genome Res"},{"key":"1905_CR40","doi-asserted-by":"publisher","first-page":"120","DOI":"10.1101\/gr.3021305","volume":"15","author":"E Axelsson","year":"2005","unstructured":"Axelsson E, Webster MT, Smith NGC, Burt DW, Ellegren H. Comparison of the chicken and turkey genomes reveals a higher rate of nucleotide divergence on microchromosomes than macrochromosomes. Genome Res. 2005;15:120\u20135.","journal-title":"Genome Res"},{"key":"1905_CR41","doi-asserted-by":"publisher","first-page":"285","DOI":"10.1146\/annurev-genom-082908-150001","volume":"10","author":"L Duret","year":"2009","unstructured":"Duret L, Galtier N. Biased gene conversion and the evolution of mammalian genomic landscapes. Annu Rev Genomics Hum Genet. 2009;10:285\u2013311.","journal-title":"Annu Rev Genomics Hum Genet"},{"key":"1905_CR42","doi-asserted-by":"publisher","first-page":"1181","DOI":"10.1093\/oxfordjournals.molbev.a004176","volume":"19","author":"JA Birdsell","year":"2002","unstructured":"Birdsell JA. Integrating genomics, bioinformatics, and classical genetics to study the effects of recombination on genome evolution. Mol Biol Evol. 2002;19:1181\u201397.","journal-title":"Mol Biol Evol"},{"key":"1905_CR43","doi-asserted-by":"publisher","first-page":"1420","DOI":"10.1101\/gr.6395807","volume":"17","author":"TR Dreszer","year":"2007","unstructured":"Dreszer TR, Wall GD, Haussler D, Pollard KS. Biased clustered substitutions in the human genome: the footprints of male-driven biased gene conversion. Genome Res. 2007;17:1420\u201330.","journal-title":"Genome Res"},{"key":"1905_CR44","doi-asserted-by":"crossref","unstructured":"Berglund J, Pollard KS, Webster MT. Hotspots of biased nucleotide substitutions in human genes. PLoS Biol. 2009;7:e26.","DOI":"10.1371\/journal.pbio.1000026"},{"key":"1905_CR45","doi-asserted-by":"publisher","first-page":"1001","DOI":"10.1101\/gr.104372.109","volume":"20","author":"J Romiguier","year":"2010","unstructured":"Romiguier J, Ranwez V, Douzery EJP, Galtier N. Contrasting GC-content dynamics across 33 mammalian genomes: relationship with life-history traits and chromosome sizes. Genome Res. 2010;20:1001\u20139.","journal-title":"Genome Res"},{"key":"1905_CR46","doi-asserted-by":"publisher","first-page":"516","DOI":"10.1093\/gbe\/evr051","volume":"3","author":"JA Capra","year":"2011","unstructured":"Capra JA, Pollard KS. Substitution patterns are GC-biased in divergent sequences across the metazoans. Genome Biol Evol. 2011;3:516\u201327.","journal-title":"Genome Biol Evol"},{"key":"1905_CR47","doi-asserted-by":"publisher","first-page":"240","DOI":"10.1093\/gbe\/evu277","volume":"7","author":"E Figuet","year":"2014","unstructured":"Figuet E, Ballenghien M, Romiguier J, Galtier N. Biased gene conversion and GC-content evolution in the coding sequences of reptiles and vertebrates. Genome Biol Evol. 2014;7:240\u201350.","journal-title":"Genome Biol Evol"},{"key":"1905_CR48","doi-asserted-by":"publisher","first-page":"675","DOI":"10.1093\/gbe\/evs052","volume":"4","author":"E Pessia","year":"2012","unstructured":"Pessia E, Popa A, Mousset S, Rezvoy C, Duret L, Marais GAB. Evidence for widespread GC-biased gene conversion in eukaryotes. Genome Biol Evol. 2012;4:675\u201382.","journal-title":"Genome Biol Evol"},{"key":"1905_CR49","doi-asserted-by":"publisher","first-page":"239","DOI":"10.1146\/annurev-ecolsys-110411-160327","volume":"44","author":"H Ellegren","year":"2013","unstructured":"Ellegren H. The evolutionary genomics of birds. Annu Rev Ecol Evol Syst. 2013;44:239\u201359.","journal-title":"Annu Rev Ecol Evol Syst"},{"key":"1905_CR50","doi-asserted-by":"publisher","first-page":"549","DOI":"10.1186\/s13059-014-0549-1","volume":"15","author":"CC Weber","year":"2014","unstructured":"Weber CC, Boussau B, Romiguier J, Jarvis ED, Ellegren H. Evidence for GC-biased gene conversion as a driver of between-lineage differences in avian base composition. Genome Biol. 2014;15:549.","journal-title":"Genome Biol"},{"key":"1905_CR51","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1007\/s00412-018-0685-6","volume":"128","author":"RE O\u2019Connor","year":"2019","unstructured":"O\u2019Connor RE, Kiazim L, Skinner B, Fonseka G, Joseph S, Jennings R, et al. Patterns of microchromosome organization remain highly conserved throughout avian evolution. Chromosoma. 2019;128:21\u20139.","journal-title":"Chromosoma"},{"key":"1905_CR52","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1186\/s12864-018-5378-2","volume":"20","author":"VN Laine","year":"2019","unstructured":"Laine VN, Gossmann TI, van Oers K, Visser ME, Groenen MAM. Exploring the unmapped DNA and RNA reads in a songbird genome. BMC Genomics. 2019;20:19.","journal-title":"BMC Genomics"},{"key":"1905_CR53","doi-asserted-by":"publisher","first-page":"2594","DOI":"10.1074\/jbc.271.5.2594","volume":"271","author":"S Baqu\u00e9","year":"1996","unstructured":"Baqu\u00e9 S, Guinovart JJ, G\u00f3mez-Foix AM. Overexpression of muscle glycogen phosphorylase in cultured human muscle fibers causes increased glucose consumption and nonoxidative disposal. J Biol Chem. 1996;271:2594\u20138.","journal-title":"J Biol Chem"},{"key":"1905_CR54","doi-asserted-by":"crossref","unstructured":"Richter EA, Hargreaves M. Exercise, GLUT4, and skeletal muscle glucose uptake. Physiol Rev. 2013;93:993\u20131017.","DOI":"10.1152\/physrev.00038.2012"},{"key":"1905_CR55","doi-asserted-by":"publisher","first-page":"645","DOI":"10.1007\/PL00000887","volume":"58","author":"FM Carver","year":"2001","unstructured":"Carver FM, Shibley IA Jr, Pennington JS, Pennington SN. Differential expression of glucose transporters during chick embryogenesis. Cell Mol Life Sci C. 2001;58:645\u201352.","journal-title":"Cell Mol Life Sci C"},{"key":"1905_CR56","doi-asserted-by":"publisher","first-page":"80","DOI":"10.1016\/S0016-6480(03)00145-X","volume":"133","author":"Y Seki","year":"2003","unstructured":"Seki Y, Sato K, Kono T, Abe H, Akiba Y. Broiler chickens (Ross strain) lack insulin-responsive glucose transporter GLUT4 and have GLUT8 cDNA. Gen Comp Endocrinol. 2003;133:80\u20137.","journal-title":"Gen Comp Endocrinol"},{"key":"1905_CR57","doi-asserted-by":"publisher","first-page":"510","DOI":"10.1080\/00071660500181289","volume":"46","author":"T Kono","year":"2005","unstructured":"Kono T, Nishida M, Nishiki Y, Seki Y, Sato K, Akiba Y. Characterisation of glucose transporter (GLUT) gene expression in broiler chickens. Br Poult Sci. 2005;46:510\u20135.","journal-title":"Br Poult Sci"},{"key":"1905_CR58","doi-asserted-by":"publisher","first-page":"263","DOI":"10.1016\/j.cbpb.2005.12.027","volume":"144","author":"KL Sweazea","year":"2006","unstructured":"Sweazea KL, Braun EJ. Glucose transporter expression in English sparrows (Passer domesticus). Comp Biochem Physiol B. 2006;144:263\u201370.","journal-title":"Comp Biochem Physiol B"},{"key":"1905_CR59","doi-asserted-by":"crossref","unstructured":"Welch KC, Allalou A, Sehgal P, Cheng J, Ashok A. Glucose transporter expression in an avian nectarivore: the ruby-throated hummingbird (Archilochus colubris). PLoS ONE. 2013;8:e77003.","DOI":"10.1371\/journal.pone.0077003"},{"key":"1905_CR60","doi-asserted-by":"crossref","unstructured":"Birnbaum MJ, GLUT-4. Identification of a novel gene encoding an insulin-responsive glucose transporter protein. Cell. 1989;57:305\u201315.","DOI":"10.1016\/0092-8674(89)90968-9"},{"key":"1905_CR61","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pone.0139517","volume":"10","author":"E Coudert","year":"2015","unstructured":"Coudert E, Pascal G, Dupont J, Simon J, Cailleau-Audouin E, Crochet S, et al. Phylogenesis and biological characterization of a new glucose transporter in the chicken (Gallus gallus), GLUT12. PLoS ONE. 2015;10:1\u201318.","journal-title":"PLoS ONE"},{"key":"1905_CR62","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1016\/j.cbpc.2005.01.008","volume":"141","author":"Y Tokushima","year":"2005","unstructured":"Tokushima Y, Takahashi K, Sato K, Akiba Y. Glucose uptake in vivo in skeletal muscles of insulin-injected chicks. Comp Biochem Physiol B. 2005;141:43\u20138.","journal-title":"Comp Biochem Physiol B"},{"key":"1905_CR63","doi-asserted-by":"publisher","first-page":"431","DOI":"10.1007\/s00359-017-1150-3","volume":"203","author":"S Jenni-Eiermann","year":"2017","unstructured":"Jenni-Eiermann S. Energy metabolism during endurance flight and the post-flight recovery phase. J Comp Physiol A. 2017;203:431\u20138.","journal-title":"J Comp Physiol A"},{"key":"1905_CR64","doi-asserted-by":"publisher","first-page":"424","DOI":"10.1080\/713654969","volume":"41","author":"J Simon","year":"2000","unstructured":"Simon J, Guillaumin S, Chevalier B, Derouet M, Guy G, Marche G, et al. Plasma glucose-insulin relationship in chicken lines selected for high or low fasting glycaemia. Br Poult Sci. 2000;41:424\u20139.","journal-title":"Br Poult Sci"},{"key":"1905_CR65","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1016\/j.arr.2009.07.006","volume":"9","author":"J Munshi-South","year":"2010","unstructured":"Munshi-South J, Wilkinson GS. Bats and birds: exceptional longevity despite high metabolic rates. Ageing Res Rev. 2010;9:12\u20139.","journal-title":"Ageing Res Rev"},{"key":"1905_CR66","doi-asserted-by":"publisher","first-page":"273","DOI":"10.1111\/j.1474-9726.2009.00542.x","volume":"9","author":"RE Ricklefs","year":"2010","unstructured":"Ricklefs RE. Insights from comparative analyses of aging in birds and mammals. Aging Cell. 2010;9:273\u201384.","journal-title":"Aging Cell"},{"key":"1905_CR67","doi-asserted-by":"publisher","first-page":"411","DOI":"10.1016\/0005-2795(81)90207-5","volume":"667","author":"CM Schettino","year":"1981","unstructured":"Schettino CM, Lima DF, Leyton JF, El-Dorry HA, Bacila M. Studies on the structure of aldolase A from chicken muscle. Biochim Biophys Acta. 1981;667:411\u201320.","journal-title":"Biochim Biophys Acta"},{"key":"1905_CR68","doi-asserted-by":"publisher","first-page":"554","DOI":"10.1093\/oxfordjournals.jbchem.a124743","volume":"117","author":"M Tanaka","year":"1995","unstructured":"Tanaka M, Maeda K, Nakashima K. Chicken \u03b1-enolase but not \u03b2-enolase has a src-dependent tyrosine-phosphorylation site: cDNA cloning and nucleotide sequence analysis. J Biochem. 1995;117:554\u20139.","journal-title":"J Biochem"},{"key":"1905_CR69","doi-asserted-by":"publisher","first-page":"232","DOI":"10.1016\/0304-4165(85)90027-3","volume":"841","author":"PM Sokolove","year":"1985","unstructured":"Sokolove PM. Altered membrane association of glycogen phosphorylase in the dystrophic chicken. Biochim Biophys Acta. 1985;841:232\u20136.","journal-title":"Biochim Biophys Acta"},{"key":"1905_CR70","doi-asserted-by":"crossref","unstructured":"Lemaire K, Moura RF, Granvik M, Igoillo-Esteve M, Hohmeier HE, Hendrickx N, et al. Ubiquitin fold modifier 1 (UFM1) and its target UFBP1 protect pancreatic beta cells from ER stress-induced apoptosis. PLoS ONE. 2011;6:e18517.","DOI":"10.1371\/journal.pone.0018517"},{"key":"1905_CR71","doi-asserted-by":"publisher","first-page":"45e","DOI":"10.1093\/nar\/29.9.e45","volume":"29","author":"MW Pfaffl","year":"2001","unstructured":"Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29:45e\u201345.","journal-title":"Nucleic Acids Res"},{"key":"1905_CR72","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1038\/sj.cr.7290122","volume":"12","author":"YX Hu","year":"2002","unstructured":"Hu YX, Guo JY, Shen L, Chen Y, Zhang ZC, Zhang YL. Get effective polyclonal antisera in one month. Cell Res. 2002;12:157\u201360.","journal-title":"Cell Res"},{"key":"1905_CR73","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1016\/0003-2697(84)90782-6","volume":"138","author":"D Wessel","year":"1984","unstructured":"Wessel D, Fl\u00fcgge UI. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem. 1984;138:141\u20133.","journal-title":"Anal Biochem"},{"key":"1905_CR74","doi-asserted-by":"crossref","unstructured":"Thorrez L, Van Deun K, Tranchevent L-C, Van Lommel L, Engelen K, Marchal K, et al. Using ribosomal protein genes as reference: a tale of caution. PLoS ONE. 2008;3:e1854.","DOI":"10.1371\/journal.pone.0001854"}],"container-title":["BMC Ecology and Evolution"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12862-021-01905-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s12862-021-01905-7\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12862-021-01905-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,2,6]],"date-time":"2023-02-06T17:03:42Z","timestamp":1675703022000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcevolbiol.biomedcentral.com\/articles\/10.1186\/s12862-021-01905-7"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,9,18]]},"references-count":74,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["1905"],"URL":"https:\/\/doi.org\/10.1186\/s12862-021-01905-7","relation":{},"ISSN":["2730-7182"],"issn-type":[{"value":"2730-7182","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,9,18]]},"assertion":[{"value":"16 March 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"31 August 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 September 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The ethical committee of the KU Leuven approved the experiments performed on the animals (Project Number 124\/2012).","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"176"}}