Kiwi genome provides insights into evolution of a nocturnal lifestyle

Genome Biology

Volumn 16, Issue 1, 2015, Pages

  Le Duc, Diana ^a,b   Renaud, Gabriel ^b   Krishnan, Arunkumar ^c   Almén, Markus Sällman ^c   Huynen, Leon ^d   Prohaska, Sonja J ^a   Ongyerth, Matthias ^b   Bitarello, Bárbara D ^e   Schiöth, Helgi B ^c   Hofreiter, Michael ^f   Stadler, Peter F ^a   Prüfer, Kay ^b   Lambert, David ^d   Kelso, Janet ^b   Schöneberg, Torsten ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^c UPPSALA UNIVERSITY   (Sweden)

^d GRIFFITH UNIVERSITY   (Australia)

^e UNIVERSITY OF SÃO PAULO   (Brazil)

^f UNIVERSITY OF POTSDAM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MELANOPSIN; NEUROPSIN;

ADAPTATION; APTERYX MANTELLI; ARTICLE; BIRD; CONTROLLED STUDY; FEMALE; FORAGING; GALLOANSERAE; GENE; GENE INACTIVATION; GENOME; LIFESTYLE; MULTIGENE FAMILY; NATURAL SELECTION; NEOAVES; NEW ZEALAND; NONHUMAN; OLFACTORY RECEPTOR; OLIGOCENE; OPN1LW GENE; OPN1SW GENE; OPN3 GENE; OPN4 1 GENE; OPN4 2 GENE; OPN5 GENE; OPSIN VA LIKE GENE; RATITE; RHO GENE; SEQUENCE ANALYSIS; SMELLING; SONGBIRD; SWS2 GENE; VISION; ANATOMY AND HISTOLOGY; ANIMAL; DARKNESS; GENETIC SELECTION; GENETICS; GENOMICS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; ODOR;

APTERYX; APTERYX AUSTRALIS; AVES; MAMMALIA;

ADAPTATION, BIOLOGICAL; ANIMALS; DARKNESS; EVOLUTION, MOLECULAR; GENOME; GENOMICS; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PALAEOGNATHAE; SELECTION, GENETIC; SMELL; VISION, OCULAR;

EID: 84937677238     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-015-0711-4     Document Type: Article

References (91)

1. Bunce M, Worthy TH, Phillips MJ, Holdaway RN, Willerslev E, Haile J, et al. The evolutionary history of the extinct ratite moa and New Zealand Neogene paleogeography. Proc Natl Acad Sci U S A. 2009;106:20646-51.
2. Iviartin GR. Sensory capacities and the nocturnal habit of owls (Strigiformes). IBIS. 1986;128:266-77.
3. Corfield JR, Parsons S, Harimoto Y, Acosta ML. Retinal anatomy of the New Zealand kiwi: structural traits consistent with their nocturnal behavior. Anat Rec (Hoboken). 2015;298:771-9.
4. Gerkema MP, Davies WI, Foster RG, Menaker M, Hut RA. The nocturnal bottleneck and the evolution of activity patterns in mammals. Proc Biol Sci. 2013;280:20130508.
5. Kelley DR, Schatz MC, Salzberg SL. Quake: quality-aware detection and correction of sequencing errors. Genome Biol. 2010;11:R116.
6. Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience. 2012;1:18.
7. 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;346:1311-20.
8. International Chicken Genome Sequencing C. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature. 2004;432:695-716.
9. Warren WC, Clayton DF, Ellegren H, Arnold AP, Hillier LW, Kunstner A, et al. The genome of a songbird. Nature. 2010;464:757-62.
10. Cantarel BL, Korf I, Robb SM, Parra G, Ross E, Moore B, et al. MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res. 2008;18:188-96.
11. Kondrashov FA. Gene duplication as a mechanism of genomic adaptation to a changing environment. Proc Biol Sci. 2012;279:5048-57.
12. Li H, Coghlan A, Ruan J, Coin LJ, Heriche JK, Osmotherly L, et al. TreeFam: a curated database of phylogenetic trees of animal gene families. Nucleic Acids Res. 2006;34:D572-80.
13. Sneddon TP, Zhe XS, Edmunds SC, Li P, Goodman L, Hunter CI. GigaDB: promoting data dissemination and reproducibility. Database (Oxford). 2014;2014:bau018.
14. Flicek P, Ahmed I, Amode MR, Barrell D, Beal K, Brent S, et al. Ensembl 2013. Nucleic Acids Res. 2013;41:D48-55.
15. Wilgenbusch JC, Swofford D. Inferring evolutionary trees with PAUP*. Curr Protoc Bioinformatics. 2003;Chapter 6:Unit 6 4.
16. Hughes AL, Friedman R. Genome size reduction in the chicken has involved massive loss of ancestral protein-coding genes. Mol Biol Evol. 2008;25:2681-8.
17. Zhan X, Pan S, Wang J, Dixon A, He J, Muller MG, et al. Peregrine and saker falcon genome sequences provide insights into evolution of a predatory lifestyle. Nat Genet. 2013;45:563-6.
18. Huang Y, Li Y, Burt DW, Chen H, Zhang Y, Qian W, et al. The duck genome and transcriptome provide insight into an avian influenza virus reservoir species. Nat Genet. 2013;45:776-83.
19. Denton JF, Lugo-Martinez J, Tucker AE, Schrider DR, Warren WC, Hahn MW. Extensive error in the number of genes inferred from draft genome assemblies. PLoS Comput Biol. 2014;10, e1003998.
20. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000;25:25-9.
21. Zakon HH, Jost MC, Lu Y. Expansion of voltage-dependent Na+ channel gene family in early tetrapods coincided with the emergence of terrestriality and increased brain complexity. Mol Biol Evol. 2011;28:1415-24.
22. Luxey M, Jungas T, Laussu J, Audouard C, Garces A, Davy A. Eph:ephrin-B1 forward signaling controls fasciculation of sensory and motor axons. Dev Biol. 2013;383:264-74.
23. Patel K, Nittenberg R, D'Souza D, Irving C, Burt D, Wilkinson DG, et al. Expression and regulation of Cek-8, a cell to cell signalling receptor in developing chick limb buds. Development. 1996;122:1147-55.
24. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007;24:1586-91.
25. Pavlidis P, Jensen JD, Stephan W, Stamatakis A. A critical assessment of storytelling: gene ontology categories and the importance of validating genomic scans. Mol Biol Evol. 2012;29:3237-48.
26. Torii M, Kojima D, Okano T, Nakamura A, Terakita A, Shichida Y, et al. Two isoforms of chicken melanopsins show blue light sensitivity. FEBS Lett. 2007;581:5327-31.
27. Martin GR, Wilson KJ, Martin Wild J, Parsons S, Fabiana Kubke M, Corfield J. Kiwi forego vision in the guidance of their nocturnal activities. PLoS One. 2007;2, e198.
28. Osorio D, Vorobyev M. A review of the evolution of animal colour vision and visual communication signals. Vision research. 2008;48:2042-51.
29. Beukers MW, Kristiansen I, IJzerman AP, Edvardsen I. TinyGRAP database: a bioinformatics tool to mine G-protein-coupled receptor mutant data. Trends Pharmacol Sci. 1999;20:475-7.
30. Jansen JJ, Mulder WR, De Caluwe GL, Vlak JM, De Grip WJ. In vitro expression of bovine opsin using recombinant baculovirus: the role of glutamic acid (134) in opsin biosynthesis and glycosylation. Biochim Biophys Acta. 1991;1089:68-76.
31. Capra V, Veltri A, Foglia C, Crimaldi L, Habib A, Parenti M, et al. Mutational analysis of the highly conserved ERY motif of the thromboxane A2 receptor: alternative role in G protein-coupled receptor signaling. Mol Pharmacol. 2004;66:880-9.
32. Schulz A, Schoneberg T, Paschke R, Schultz G, Gudermann T. Role of the third intracellular loop for the activation of gonadotropin receptors. Mol Endocrinol. 1999;13:181-90.
33. Vogel R, Mahalingam M, Ludeke S, Huber T, Siebert F, Sakmar TP. Functional role of the "ionic lock"--an interhelical hydrogen-bond network in family A heptahelical receptors. J Mol Biol. 2008;380:648-55.
34. Ebrey T, Koutalos Y. Vertebrate photoreceptors. Prog Retin Eye Res. 2001;20:49-94.
35. Schoneberg T, Schulz A, Biebermann H, Hermsdorf T, Rompler H, Sangkuhl K. Mutant G-protein-coupled receptors as a cause of human diseases. Pharmacol Ther. 2004;104:173-206.
36. Tao YX. Inactivating mutations of G protein-coupled receptors and diseases: structure-function insights and therapeutic implications. Pharmacol Ther. 2006;111:949-73.
37. Vassart G, Costagliola S. G protein-coupled receptors: mutations and endocrine diseases. Nat Rev Endocrinol. 2011;7:362-72.
38. Mitchell KJ, Llamas B, Soubrier J, Rawlence NJ, Worthy TH, Wood J, et al. Ancient DNA reveals elephant birds and kiwi are sister taxa and clarifies ratite bird evolution. Science. 2014;344:898-900.
39. Corfield JR, Eisthen HL, Iwaniuk AN, Parsons S. Anatomical specializations for enhanced olfactory sensitivity in kiwi, Apteryx mantelli. Brain Behav Evol. 2014;84:214-26.
40. Niimura Y, Nei M. Extensive gains and losses of olfactory receptor genes in mammalian evolution. PLoS One. 2007;2, e708.
41. Hasin-Brumshtein Y, Lancet D, Olender T. Human olfaction: from genomic variation to phenotypic diversity. Trends Genet. 2009;25:178-84.
42. Steiger SS, Fidler AE, Kempenaers B. Evidence for increased olfactory receptor gene repertoire size in two nocturnal bird species with well-developed olfactory ability. BMC Evol Biol. 2009;9:117.
43. Preston GM. Cloning gene family members using PCR with degenerate oligonucleotide primers. In: White BA (ed.) PCR cloning protocols: from molecular cloning to genetic engineering; In series: Methods in molecular biology (Clifton, N.J.) 67; Humana Press: 1997 pg 433-49. ISBN 0896034436
44. Liu S, Wei W, Chu Y, Zhang L, Shen J, An C. De novo transcriptome analysis of wing development-related signaling pathways in Locusta migratoria manilensis and Ostrinia furnacalis (Guenee). PLoS One. 2014;9, e106770.
45. Steiger SS, Kuryshev VY, Stensmyr MC, Kempenaers B, Mueller JC. A comparison of reptilian and avian olfactory receptor gene repertoires: species-specific expansion of group gamma genes in birds. BMC Genomics. 2009;10:446.
46. Morrison SS, Pyzh R, Jeon MS, Amaro C, Roig FJ, Baker-Austin C, et al. Impact of analytic provenance in genome analysis. BMC Genomics. 2014;15:S1.
47. Margulies DH, Natarajan K, Rossjohn J, McCluskey J. Fundamental Immunology. 7th ed. Philadelphia, PA: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2012. p. 511.
48. Shannon CE. The mathematical theory of communication. Bell System Tech J. 1948;27:379-243. 623-56.
49. Litwin S, Jores R. Shannon information as a measure of amino acid diversity. In: Perelson AS, Weisbuch G, editors. Theoretical and experimental insights into immunology, vol. 66. NATO ASI Series. Berlin: Springer Berlin Heidelberg; 1992. p. 279-87.
50. McNab BK. Resource use and the survival of land and freshwater vertebrates on oceanic islands. American Naturalist. 1994;144:643-60.
51. Cooper A, Cooper RA. The Oligocene bottleneck and New Zealand biota: genetic record of a past environmental crisis. Proc Biol Sci. 1995;261:293-302.
52. Grzimek B, Schlager N, Olendorf D, McDade MC. Grzimek's animal life encyclopedia. Gale: Gale, MI; 2004.
53. Tanaka M. Molecular and evolutionary basis of limb field specification and limb initiation. Dev Growth Differ. 2013;55:149-63.
54. Pascual-Anaya J, D'Aniello S, Kuratani S, Garcia-Fernandez J. Evolution of Hox gene clusters in deuterostomes. BMC Dev Biol. 2013;13:26.
55. Dimitrieva S, Bucher P. UCNEbase--a database of ultraconserved non-coding elements and genomic regulatory blocks. Nucleic Acids Res. 2013;41:D101-9.
56. Woolfe A, Elgar G. Organization of conserved elements near key developmental regulators in vertebrate genomes. Adv Genet. 2008;61:307-38.
57. Pennacchio LA, Ahituv N, Moses AM, Prabhakar S, Nobrega MA, Shoukry M, et al. In vivo enhancer analysis of human conserved non-coding sequences. Nature. 2006;444:499-502.
58. Bell SM, Schreiner CM, Waclaw RR, Campbell K, Potter SS, Scott WJ. Sp8 is crucial for limb outgrowth and neuropore closure. Proc Natl Acad Sci U S A. 2003;100:12195-200.
59. Gestri G, Osborne RJ, Wyatt AW, Gerrelli D, Gribble S, Stewart H, et al. Reduced TFAP2A function causes variable optic fissure closure and retinal defects and sensitizes eye development to mutations in other morphogenetic regulators. Hum Genet. 2009;126:791-803.
60. Reid B, Williams GR. The kiwi. In: Kuschel G, editor. Biogeography and Ecology in New Zealand, vol. 27. The Hague: Springer Netherlands; 1975. p. 301-30.
61. van Tuinen M, Sibley CG, Hedges SB. Phylogeny and biogeography of ratite birds inferred from DNA sequences of the mitochondrial ribosomal genes. Mol Biol Evol. 1998;15:370-6.
62. Hackett SJ, Kimball RT, Reddy S, Bowie RC, Braun EL, Braun MJ, et al. A phylogenomic study of birds reveals their evolutionary history. Science. 2008;320:1763-8.
63. Worthy TH, Worthy JP, Tennyson AJD, Salisbury SW, Hand SJ, Scofield RP. Miocene fossils show that kiwi (Apteryx, Apterygidae) are probably not phyletic dwarves. In: Göhlich UB, Kroh A, editors. Proceedings of the 8th International Meeting Society of Avian Paleontology and Evolution. Vienna, 2012, Verlag des Naturhistorischen Museums in Wien, Vienna; 2013. p. 63-80.
64. Jacobs GH. Losses of functional opsin genes, short-wavelength cone photopigments, and color vision--a significant trend in the evolution of mammalian vision. Vis Neurosci. 2013;30:39-53.
65. Striedter GF. Principles of brain evolution. Sinauer Associates Inc.,U.S. ISBN: 978-0-87893-820-9. 2004/2005
66. Walls GL. The vertebrate eye and its adaptive radiation. Oxford: Cranbook Institute of Science; 1942.
67. Crompton AW, Taylor CR, Jagger JA. Evolution of homeothermy in mammals. Nature. 1978;272:333-6.
68. McNab BK. Metabolism and temperature regulation of kiwis (Apterygidae). The Auk. 1996;113:687-92.
69. Sales J. The endangered kiwi: a review. Folia Zoologica Praha. 2005;54:1.
70. Brooke ML, Hanley S, Laughlin SB. The scaling of eye size with body mass in birds. Proc Biol Sci. 1999;266:405-12.
71. Hall MI, Kamilar JM, Kirk EC. Eye shape and the nocturnal bottleneck of mammals. Proc Biol Sci. 2012;279:4962-8.
72. Cunningham S, Castro I, Alley M. A new prey-detection mechanism for kiwi (Apteryx spp.) suggests convergent evolution between paleognathous and neognathous birds. J Anat. 2007;211:493-502.
73. Gilad Y, Przeworski M, Lancet D. Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates. PLoS Biol. 2004;2, E5.
74. Stanke M, Keller O, Gunduz I, Hayes A, Waack S, Morgenstern B. AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 2006;34:W435-9.
75. Gertz EM, Yu YK, Agarwala R, Schaffer AA, Altschul SF. Composition-based statistics and translated nucleotide searches: improving the TBLASTN module of BLAST. BMC Biol. 2006;4:41.
76. Prüfer K, Muetzel B, Do HH, Weiss G, Khaitovich P, Rahm E, et al. FUNC: a package for detecting significant associations between gene sets and ontological annotations. BMC Bioinform. 2007;8:41.
77. De Bie T, Cristianini N, Demuth JP, Hahn MW. CAFE: a computational tool for the study of gene family evolution. Bioinformatics. 2006;22:1269-71.
78. Bindea G, Mlecnik B, Hackl H, Charoentong P, Tosolini M, Kirilovsky A, et al. ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics. 2009;25:1091-3.
79. Kall L, Krogh A, Sonnhammer EL. An HMM posterior decoder for sequence feature prediction that includes homology information. Bioinformatics. 2005;21:i251-7.
80. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25:2078-9.
81. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772-80.
82. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 1999;41:95-8.
83. Yang Z. Computational Molecular Evolution. Oxford: Oxford University Press; 2006.
84. Prohaska SJ, Fried C, Flamm C, Wagner GP, Stadler PF. Surveying phylogenetic footprints in large gene clusters: applications to Hox cluster duplications. Mol Phylogenet Evol. 2004;31:581-604.
85. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403-10.
86. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792-7.
87. Kiwi Genome. Available at: http://www.bioinf.uni-leipzig.de/~studla/KIWI-HOX/.
88. Kiwi Annotated HOX Cluster. Available at: https://bioinf.eva.mpg.de/KIWI-HOX/
89. Kiwi Annotated UCNEs. Available at: https://bioinf.eva.mpg.de/KIWI-UCNEs/
90. Ellegren H, Smeds L, Burri R, Olason PI, Backstrom N, Kawakami T, et al. The genomic landscape of species divergence in Ficedula flycatchers. Nature. 2012;491:756-60.
91. Dalloul RA, Long JA, Zimin AV, Aslam L, Beal K, Le Blomberg A, et al. Multi-platform next-generation sequencing of the domestic turkey (Meleagris gallopavo): genome assembly and analysis. PLoS Biol. 2010;8:1-21.