New genome assembly of the barn owl (Tyto alba alba)

Abstract New genomic tools open doors to study ecology, evolution, and population genomics of wild animals. For the Barn owl species complex, a cosmopolitan nocturnal raptor, a very fragmented draft genome was assembled for the American species (Tyto furcata pratincola) (Jarvis et al. 2014). To improve the genome, we assembled de novo Illumina and Pacific Biosciences (PacBio) long reads sequences of its European counterpart (Tyto alba alba). This genome assembly of 1.219 Gbp comprises 21,509 scaffolds and results in a N50 of 4,615,526 bp. BUSCO (Universal Single‐Copy Orthologs) analysis revealed an assembly completeness of 94.8% with only 1.8% of the genes missing out of 4,915 avian orthologs searched, a proportion similar to that found in the genomes of the zebra finch (Taeniopygia guttata) or the collared flycatcher (Ficedula albicollis). By mapping the reads of the female American barn owl to the male European barn owl reads, we detected several structural variants and identified 70 Mbp of the Z chromosome. The barn owl scaffolds were further mapped to the chromosomes of the zebra finch. In addition, the completeness of the European barn owl genome is demonstrated with 94 of 128 proteins missing in the chicken genome retrieved in the European barn owl transcripts. This improved genome will help future barn owl population genomic investigations.

[1]  A. Roulin,et al.  Geographical variation in bill size provides evidence for Allen’s rule in a cosmopolitan raptor , 2019, Global Ecology and Biogeography.

[2]  A. Roulin,et al.  Differential fitness effects of moonlight on plumage colour morphs in barn owls , 2019, Nature Ecology & Evolution.

[3]  S. Mirarab,et al.  Phylogenetic Signal of Indels and the Neoavian Radiation , 2019, Diversity.

[4]  Alexey M. Kozlov,et al.  RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference , 2019, Bioinform..

[5]  Natasha I. Bloch,et al.  Owls lack UV-sensitive cone opsin and red oil droplets, but see UV light at night: Retinal transcriptomes and ocular media transmittance , 2019, Vision Research.

[6]  A. Roulin,et al.  Climate-driven convergent evolution of plumage colour in a cosmopolitan bird , 2019, Global Ecology and Biogeography.

[7]  Jia-kuan Chen,et al.  Incomplete lineage sorting and introgression in the diversification of Chinese spot-billed ducks and mallards , 2018, Current zoology.

[8]  D. Larkin,et al.  Germline-restricted chromosome (GRC) is widespread among songbirds , 2018, Proceedings of the National Academy of Sciences.

[9]  D. Griffin,et al.  Chromosome-level assembly reveals extensive rearrangement in saker falcon and budgerigar, but not ostrich, genomes , 2018, Genome Biology.

[10]  Alex Warwick Vesztrocy,et al.  OMA standalone: orthology inference among public and custom genomes and transcriptomes , 2018, bioRxiv.

[11]  Alexander Suh,et al.  How complete are “complete” genome assemblies?—An avian perspective , 2018, Molecular ecology resources.

[12]  A. Roulin,et al.  Comprehensive molecular phylogeny of barn owls and relatives (Family: Tytonidae), and their six major Pleistocene radiations. , 2018, Molecular phylogenetics and evolution.

[13]  Kathryn C Asalone,et al.  Discovery of the First Germline-Restricted Gene by Subtractive Transcriptomic Analysis in the Zebra Finch, Taeniopygia guttata , 2018, Current Biology.

[14]  J. G. Burleigh,et al.  Comparison of the Chinese bamboo partridge and red Junglefowl genome sequences highlights the importance of demography in genome evolution , 2018, BMC Genomics.

[15]  Chao Zhang,et al.  ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees , 2018, BMC Bioinformatics.

[16]  Benedikt Grothe,et al.  How the Barn Owl Computes Auditory Space , 2018, Trends in Neurosciences.

[17]  N. Zhang,et al.  The first set of universal nuclear protein-coding loci markers for avian phylogenetic and population genetic studies , 2018, Scientific Reports.

[18]  H. Wagner,et al.  Development of ear asymmetry in the American barn owl (Tyto furcata pratincola). , 2017, Zoology.

[19]  Gaston H. Gonnet,et al.  The OMA orthology database in 2018: retrieving evolutionary relationships among all domains of life through richer web and programmatic interfaces , 2017, Nucleic Acids Res..

[20]  Fanny Cazettes,et al.  Emergence of an Adaptive Command for Orienting Behavior in Premotor Brainstem Neurons of Barn Owls , 2017, The Journal of Neuroscience.

[21]  A. Major,et al.  Sex determination and gonadal sex differentiation in the chicken model. , 2018, The International journal of developmental biology.

[22]  H. Wagner,et al.  Size discrimination in barn owls as compared to humans , 2018, Journal of Comparative Physiology A.

[23]  Nicolas Galtier,et al.  Avian Genomes Revisited: Hidden Genes Uncovered and the Rates versus Traits Paradox in Birds , 2017, Molecular biology and evolution.

[24]  J. Wall,et al.  Northern Spotted Owl (Strix occidentalis caurina) Genome: Divergence with the Barred Owl (Strix varia) and Characterization of Light-Associated Genes , 2017, Genome biology and evolution.

[25]  Han Fang,et al.  GenomeScope: Fast reference-free genome profiling from short reads , 2016, bioRxiv.

[26]  C. Carr,et al.  Development of auditory sensitivity in the barn owl , 2017, Journal of Comparative Physiology A.

[27]  M. Grabherr,et al.  Correspondence on Lovell et al.: identification of chicken genes previously assumed to be evolutionarily lost , 2017, Genome Biology.

[28]  E. Tseng,et al.  Normalized long read RNA sequencing in chicken reveals transcriptome complexity similar to human , 2017, BMC Genomics.

[29]  H. Wagner,et al.  Features of owl wings that promote silent flight , 2017, Interface Focus.

[30]  Hans H. Cheng,et al.  A New Chicken Genome Assembly Provides Insight into Avian Genome Structure , 2016, G3: Genes, Genomes, Genetics.

[31]  E. Hadly,et al.  Retinal transcriptome sequencing sheds light on the adaptation to nocturnal and diurnal lifestyles in raptors , 2016, Scientific Reports.

[32]  Xiuyue Zhang,et al.  Distinct patterns of simple sequence repeats and GC distribution in intragenic and intergenic regions of primate genomes , 2016, Aging.

[33]  C. Dessimoz,et al.  Phylo.io: Interactive Viewing and Comparison of Large Phylogenetic Trees on the Web , 2016, Molecular biology and evolution.

[34]  Leif Andersson,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. , 2016, Endocrinology.

[35]  J. Townsend,et al.  A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing , 2015, Nature.

[36]  Yun Sung Cho,et al.  The first whole genome and transcriptome of the cinereous vulture reveals adaptation in the gastric and immune defense systems and possible convergent evolution between the Old and New World vultures , 2015, Genome Biology.

[37]  Evgeny M. Zdobnov,et al.  BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs , 2015, Bioinform..

[38]  Stephen A. Smith,et al.  Analysis of phylogenomic datasets reveals conflict, concordance, and gene duplications with examples from animals and plants , 2015, BMC Evolutionary Biology.

[39]  H. Ellegren,et al.  The Dynamics of Incomplete Lineage Sorting across the Ancient Adaptive Radiation of Neoavian Birds , 2015, PLoS biology.

[40]  Sonja J. Prohaska,et al.  Kiwi genome provides insights into evolution of a nocturnal lifestyle , 2015, Genome Biology.

[41]  A. von Haeseler,et al.  IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies , 2014, Molecular biology and evolution.

[42]  Morgan Wirthlin,et al.  Conserved syntenic clusters of protein coding genes are missing in birds , 2014, Genome Biology.

[43]  Md. Shamsuzzoha Bayzid,et al.  Whole-genome analyses resolve early branches in the tree of life of modern birds , 2014, Science.

[44]  Pall I. Olason,et al.  A high-density linkage map enables a second-generation collared flycatcher genome assembly and reveals the patterns of avian recombination rate variation and chromosomal evolution , 2014, Molecular ecology.

[45]  Colin N. Dewey,et al.  De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis , 2013, Nature Protocols.

[46]  Jing He,et al.  Peregrine and saker falcon genome sequences provide insights into evolution of a predatory lifestyle , 2013, Nature Genetics.

[47]  K. Katoh,et al.  MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability , 2013, Molecular biology and evolution.

[48]  Jian Wang,et al.  SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler , 2012, GigaScience.

[49]  Hermann Wagner,et al.  Night vision in barn owls: visual acuity and contrast sensitivity under dark adaptation. , 2012, Journal of vision.

[50]  R. Gibbs,et al.  Mind the Gap: Upgrading Genomes with Pacific Biosciences RS Long-Read Sequencing Technology , 2012, PloS one.

[51]  Shinichi Nakagawa,et al.  The long and the short of avian W chromosomes: no evidence for gradual W shortening , 2012, Biology Letters.

[52]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[53]  A. Ducrest,et al.  Association between melanism, physiology and behaviour: a role for the melanocortin system. , 2011, European journal of pharmacology.

[54]  Steven J. M. Jones,et al.  Circos: an information aesthetic for comparative genomics. , 2009, Genome research.

[55]  H. Stenmark.  Rab GTPases as coordinators of vesicle traffic , 2009, Nature Reviews Molecular Cell Biology.

[56]  Toni Gabaldón,et al.  trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses , 2009, Bioinform..

[57]  Florian Odronitz,et al.  Scipio: Using protein sequences to determine the precise exon/intron structures of genes and their orthologs in closely related species , 2008, BMC Bioinformatics.

[58]  Burkhard Morgenstern,et al.  Gene prediction in eukaryotes with a generalized hidden Markov model that uses hints from external sources , 2006, BMC Bioinformatics.

[59]  E. Eichler,et al.  A genome-wide survey of structural variation between human and chimpanzee. , 2005, Genome research.

[60]  Simon Kasif,et al.  GC/AT-content spikes as genomic punctuation marks. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[61]  W. J. Kent,et al.  BLAT--the BLAST-like alignment tool. , 2002, Genome research.

[62]  D. Cavallo,et al.  Evaluation of interspecific DNA content variations and sex identification in Falconiformes and Strigiformes by flow cytometric analysis. , 1994, Cytometry.

[63]  K. Rebholz,et al.  Kinetics of enzymes with iso-mechanisms: analysis of product inhibition. , 1993, The Biochemical journal.

[64]  D. Lipman,et al.  Improved tools for biological sequence comparison. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[65]  E. Capanna,et al.  Size and structure of the bird genome--I. DNA content of 48 species of Neognathae. , 1986, Comparative biochemistry and physiology. B, Comparative biochemistry.