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The Wild Species Genome Ancestry of Domestic Chickens 2 3 Authors: 4 Raman Akinyanju Lawal1,2,#, Simon H

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The Wild Species Genome Ancestry of Domestic Chickens 2 3 Authors: 4 Raman Akinyanju Lawal1,2,#, Simon H bioRxiv preprint doi: https://doi.org/10.1101/711366; this version posted July 31, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 The wild species genome ancestry of domestic chickens 2 3 Authors: 4 Raman Akinyanju Lawal1,2,#, Simon H. Martin3,4, #, Koen Vanmechelen5, Addie Vereijken6, 5 Pradeepa Silva7, Raed Mahmoud Al-Atiyat8, Riyadh Salah Aljumaah9, Joram M. Mwacharo10, 6 Dong-Dong Wu11,12, Ya-Ping Zhang11,12, Paul M. Hocking13†, Jacqueline Smith13, David 7 Wragg14 & Olivier Hanotte1, 14,15* 8 9 Affiliations: 10 1Cells, Organisms and Molecular Genetics, School of Life Sciences, University of Nottingham, 11 NG7 2RD, Nottingham, United Kingdom 12 2,#The Jackson Laboratory, 600 Main Street, Bar Harbor, ME 04609, USA 13 3, #Institute of Evolutionary Biology, University of Edinburgh, EH9 3FL, Edinburgh, United 14 Kingdom 15 4Department of Zoology, University of Cambridge, CB2 3EJ, Cambridge, United Kingdom 16 5Open University of Diversity - Mouth Foundation, Hasselt, Belgium 17 6Hendrix Genetics, Technology and Service B.V., P.O. Box 114, 5830, AC, Boxmeer, The 18 Netherlands 19 7Department of Animal Sciences, Faculty of Agriculture, University of Peradeniya, Sri Lanka 20 8Genetics and Biotechnology, Animal Science Department, Agriculture Faculty, Mutah 21 University, Karak, Jordan 22 9Department of Animal Production, King Saud University, Saudi Arabia 23 10Small Ruminant Genomics, International Centre for Agricultural Research in the Dry Areas 24 (ICARDA), P.O. Box 5689, ILRI-Ethiopia Campus, Addis Ababa, Ethiopia 25 11Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, 26 650223 Kunming, China 27 12State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of 28 Zoology, Chinese Academy of Sciences, 650223 Kunming, China. 29 13The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, 30 Easter Bush Campus, Midlothian, EH25 9RG, UK 31 14Centre for Tropical Livestock Genetics and Health, The Roslin Institute, EH25 9RG, 32 Edinburgh, UK 33 15LiveGene, International Livestock Research Institute (ILRI), P. O. 5689, Addis Ababa, 34 Ethiopia 35 36 †Deceased 37 #Present address 38 *Correspondence: [email protected] and [email protected] 39 Short title: Chicken genome ancestry 40 41 1 bioRxiv preprint doi: https://doi.org/10.1101/711366; this version posted July 31, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 42 Abstract 43 Hybridization and/or introgression play a key role in the evolutionary history of animal species. 44 It is commonly observed in several orders in wild birds. The domestic chicken Gallus gallus 45 domesticus is the commonest livestock species exploited for the benefit of mankind. The origin 46 of its diversity remains unsettled. Here, we report a genome-wide analyses for signatures of 47 introgression within domestic village chicken. We first established the genome-wide 48 phylogeny and divergence time across the genus Gallus, showing the sister relationships 49 between Grey junglefowl G. sonneratii and Ceylon junglefowl G. lafayettii and that the Green 50 junglefowl is the first diverging lineage within the genus Gallus. Then, by analysing the whole- 51 genome sequences of geographically diverse chicken populations, we reveal extensive 52 bidirectional introgression between Grey junglefowl and domestic chicken and to a much less 53 extent with Ceylon junglefowl. A single case of Green junglefowl G. varius introgression was 54 identified. These introgressed regions include biological functions related to the control of gene 55 expression. Our results show that while the Red junglefowl is the main ancestral species, 56 introgressive hybridization episodes have impacted the genome and contributed to the diversity 57 of domestic chicken, although likely at different level across its geographic range. 58 Keywords: Chicken introgression, genetic diversity, chicken domestication, chicken 59 migration, livestock, divergence time, Gallus species, interspecies hybridization, Galliformes, 60 Speciation, Evolution, ABBA BABA 61 Introduction 62 63 Despite the importance of domestic chicken Gallus gallus domesticus to human societies with 64 more than 65 billion birds raised annually to produce meat by the commercial sector [1] and 65 more than 80 million metric tons of egg produced annually for global human consumption, the 66 origin and history of the genetic diversity of this major domesticate is only partly known. The 67 Red junglefowl is the recognized maternal ancestor of domestic chicken [2, 3], with evidence 68 from mitochondrial DNA (mtDNA) supporting multiple domestication centres [4] and the 69 likely maternal contribution of several of its subspecies with the exception of G. g. bankiva (a 70 subspecies with a geographic distribution restricted to Java, Bali and Sumatra). 71 72 However, the genus Gallus comprises three others wild species which may have contributed 73 to the genetic background of domestic chicken. In South Asia, the Grey junglefowl G. 74 sonneratii is found in Southwest India and the Ceylon junglefowl G. lafayettii in Sri Lanka. In 75 South-East Asia, the Green junglefowl G. varius is endemic to Java and neighbouring islands 76 [5] (Fig. 1A). Hybridization between the Red and the Grey junglefowls in their sympatric zones 77 on the Indian subcontinent has been documented [5]. In captivity, hybridization between 78 different Gallus species has been reported [6, 7], with Morejohn (1968) successfully producing 79 F1 Red junglefowl x Grey junglefowl fertile hybrids in subsequent backcrossing with both 80 species. Red junglefowl/domestic chicken mtDNA has been found in captive Grey junglefowls 81 [8, 9] and the yellow skin phenotype is likely the result of the introgression of a Grey 82 junglefowl chromosomal fragment into domestic chicken [10]. Captive F1 hybrids between 83 female domestic chicken and male Green junglefowl, prized for their plumage colour and 84 distinct voice, are common in Indonesia where they are known as Bekisar [5]. More generally, 85 inter-species hybridization and introgression is an evolutionary process that plays a major role 86 in the genetic history of species and their adaptation [11]. It may occur in the wild, when 87 species live in sympatry, or in captivity following human intervention. While unravelling how 2 bioRxiv preprint doi: https://doi.org/10.1101/711366; this version posted July 31, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 88 it happens and detecting its signatures at the genome level is central to our understanding the 89 speciation process, inter-species hybridizations are commonly practiced in agricultural plants 90 and livestock for improving productivity [12] with hybridization also known to occur between 91 domestic and wild species in several taxa [13]. Hybridization and introgression are relatively 92 common in wild birds, including in Galliformes [6, 14-17]. For example, the genetic integrity 93 of the rock partridge Alectoris graeca is being threatened in its natural habitat through 94 hybridization with the introduced red-legged partridge A. rufa [18], and the presence of 95 Japanese quail alleles in the wild migratory common quail Coturnix coturnix reveals 96 hybridization between domestic quail and the wild relative [19]. Additionally, mtDNA and 97 nuclear microsatellite analysis indicate gene flow between Silver Pheasant Lophura 98 nycthemera and Kalij Pheasant L. leucomelanos [20]. Infertile F1 hybrids between the common 99 Pheasant Phasianus colchicus and domestic chicken have also been reported in captivity [21]. 100 101 Here, we report whole genomes analysis of indigenous domestic village chickens from 102 Ethiopia, Saudi Arabia, and Sri Lanka, together with domestic breeds from Indonesia and 103 China, European fancy chickens and the four wild junglefowl species to infer the genetic 104 contributions of different Gallus sp. to the domestic chicken genome. Our results show for the 105 first time the presence of introgressed alleles in domestic chicken from the three non-red 106 junglefowls species (Grey, Ceylon and Green). We also observed extensive introgression from 107 domestic chicken/Red junglefowl into Grey junglefowl, some introgression from domestic 108 chicken into Ceylon junglefowl but no introgression from domestic chicken to Green 109 junglefowl. While our findings support the Red junglefowl as the primary ancestor of domestic 110 chicken worldwide, they also indicate that the genome diversity of domestic chicken 111 population was subsequently reshaped and enhanced following introgression from other Gallus 112 species. 113 Results 114 Sampling, genetic structure and diversity 115 We analysed 87 whole genome sequences from domestic chickens (n = 53), Red junglefowls 116 (Red (n = 6) and Javanese red (n = 3)), Grey junglefowl (n = 3), Ceylon junglefowl (n = 8), 117 and Green junglefowl (n = 12)) and common Pheasant (n = 2)). Our dataset was
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