Genetic structure in village dogs reveals a Central Asian domestication origin

Shannon, Laura M.; Boyko, Ryan H.; Castelhano, Marta G.; Corey, Elizabeth; Hayward, Jessica J.; McLean, Corin; White, Mary H.; Said, Mounir Abi; Anita, Baddley A.; Bondjengo, Nono Ikombe; Calero, Jorge; Galov, Ana; Hedimbi, Marius; Imam, Bulu; Khalap, Rajashree; Lally, Douglas; Masta, Andrew; Oliveira, Kyle C.; Pérez, Lucía Pérez; Randall, Julia; Tâm, Nguyễn Minh; Trujillo-Cornejo, Francisco J.; Valeriano, Carlos; Sutter, Nathan B.; Todhunter, Rory J.; Bustamante, Carlos D.; Boyko, Adam R.

doi:10.1073/pnas.1516215112

Cited by 186 publications

(210 citation statements)

References 49 publications

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“…S4B), although statistical power also is reduced. Patterns of neutral heterozygosity in the village dogs fall between those of breed dogs and wolves, consistent with their intermediate effective population size and variable levels of admixture between modern and ancient breeds (25). However, the ratio of zerofold to fourfold heterozygosity in village dogs depends to some degree on the filters used and is either similar to that in breed dogs or intermediate to that of dogs and wolves (SI Appendix, Fig.…”

Section: Significancementioning

confidence: 57%

Bottlenecks and selective sweeps during domestication have increased deleterious genetic variation in dogs

Marsden

Vecchyo

O’Brien

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

274

348

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Population bottlenecks, inbreeding, and artificial selection can all, in principle, influence levels of deleterious genetic variation. However, the relative importance of each of these effects on genome-wide patterns of deleterious variation remains controversial. Domestic and wild canids offer a powerful system to address the role of these factors in influencing deleterious variation because their history is dominated by known bottlenecks and intense artificial selection. Here, we assess genome-wide patterns of deleterious variation in 90 whole-genome sequences from breed dogs, village dogs, and gray wolves. We find that the ratio of amino acid changing heterozygosity to silent heterozygosity is higher in dogs than in wolves and, on average, dogs have 2-3% higher genetic load than gray wolves. Multiple lines of evidence indicate this pattern is driven by less efficient natural selection due to bottlenecks associated with domestication and breed formation, rather than recent inbreeding. Further, we find regions of the genome implicated in selective sweeps are enriched for amino acid changing variants and Mendelian disease genes. To our knowledge, these results provide the first quantitative estimates of the increased burden of deleterious variants directly associated with domestication and have important implications for selective breeding programs and the conservation of rare and endangered species. Specifically, they highlight the costs associated with selective breeding and question the practice favoring the breeding of individuals that best fit breed standards. Our results also suggest that maintaining a large population size, rather than just avoiding inbreeding, is a critical factor for preventing the accumulation of deleterious variants.M any of the mutations that arise in genomes are weakly deleterious and reduce fitness but are not always eliminated from the population by purifying natural selection. Consequently, understanding the reasons why deleterious mutations persist in populations and the role of demographic history in this process is of considerable interest (1-9). The radiation of domestic dogs offers a unique opportunity to address these questions. Dogs were originally domesticated from ancestral gray wolf populations >15,000 y ago in a process involving one or more severe population bottlenecks (10-12). The more recent isolation of modern dog breeds, which occurred over the last 300 y, involved additional population bottlenecks, intense artificial selection, and inbreeding Fig. 1A). Although this history is predicted to have resulted in the accumulation of deleterious variants, its specific effect on genomewide patterns of deleterious variation remains unclear.Here, we use complete genome sequencing data from 46 dogs representing 34 breeds, 25 village dogs, and 19 wolves to directly examine patterns of deleterious genetic variation across the dog genome (Dataset S1). Because more than half of these data derive from our own sequencing efforts, this project represents the largest survey of dog...

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Section: Significancementioning

confidence: 57%

Bottlenecks and selective sweeps during domestication have increased deleterious genetic variation in dogs

Marsden

Vecchyo

O’Brien

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

274

348

View full text Add to dashboard Cite

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“…The indigenous status of FBDs has been explicitly assessed in Africa [9,10], the Americas [10,11], and recently also in Oceania and southern parts of Europe and Asia [10]. African FBDs were shown to be a mosaic of indigenous dogs genetically distinct from non-African breed dogs, and non-native, mixed-breed individuals [9,10].…”

Section: Introductionmentioning

confidence: 99%

On the origin of mongrels: evolutionary history of free-breeding dogs in Eurasia

et al. 2015

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Although a large part of the global domestic dog population is free-ranging and free-breeding, knowledge of genetic diversity in these free-breeding dogs (FBDs) and their ancestry relations to pure-breed dogs is limited, and the indigenous status of FBDs in Asia is still uncertain. We analyse genome-wide SNP variability of FBDs across Eurasia, and show that they display weak genetic structure and are genetically distinct from pure-breed dogs rather than constituting an admixture of breeds. Our results suggest that modern European breeds originated locally from European FBDs. East Asian and Arctic breeds show closest affinity to East Asian FBDs, and they both represent the earliest branching lineages in the phylogeny of extant Eurasian dogs. Our biogeographic reconstruction of ancestral distributions indicates a gradual westward expansion of East Asian indigenous dogs to the Middle East and Europe through Central and West Asia, providing evidence for a major expansion that shaped the patterns of genetic differentiation in modern dogs. This expansion was probably secondary and could have led to the replacement of earlier resident populations in Western Eurasia. This could explain why earlier studies based on modern DNA suggest East Asia as the region of dog origin, while ancient DNA and archaeological data point to Western Eurasia.

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“…Biometric analysis of the well-preserved Timor dog indicates a similar stature to other prehistoric and contemporary village dogs across ISEA and the Pacific (Gonzalez et al 2013). The 'village dogs' of eastern Indonesia and the Pacific appear to be morphologically unrelated to Australian dingoes and perhaps represent an entirely different dog introduction to ISEA, as has also been suggested through genetic analysis by Sacks et al (2013) and Shannon et al (2015). Thus, the zooarchaeological and genetic evidence suggests at least two different dog translocations into ISEA before 3000 BP, with dingoes reaching Australia and Southeast Asian village dogs being transported into the Pacific.…”

Section: Island Southeast Asiamentioning

confidence: 72%

New Perspectives in Southeast Asian and Pacific Prehistory

Pawley¹

2017

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terra australis 45Terra Australis reports the results of archaeological and related research within the south and east of Asia, though mainly Australia, New Guinea and island Melanesia -lands that remained terra australis incognita to generations of prehistorians. Its subject is the settlement of the diverse environments in this isolated quarter of the globe by peoples who have maintained their discrete and traditional ways of life into the recent recorded or remembered past and at times into the observable present. Copyright of the text remains with the authors, 2017. This book is copyright in all countries subscribing to the Berne convention. Apart from any fair dealing for the purpose of private study, research, criticism or review, as permitted under the Copyright Act, no part may be reproduced by any process without written permission. Inquiries should be made to the publisher. List of volumes in Terra Australis Karina ArifinFakultas Ilmu Pengetahuan Budaya, Departemen Arkeologi, Universitas Indonesia, Depok, Indonesia Robert BlustDepartment of Linguistics, University of Hawai'i, Honolulu, USA David BulbeckDepartment of Archaeology and Natural History, College of Asia and the Pacific, The Australian National University, Canberra, Australia Judith CameronDepartment of Archaeology and Natural History, College of Asia and the Pacific, The Australian National University, Canberra, Australia Zhang ChiSchool of Archaeology and Museology, Peking University, Beijing, China Gang HeThe Cultural Relics and Archeological Research Institution in Hunan Province, China Helen HeathDepartment of Anthropology and Archaeology, University of Otago, North Dunedin, New Zealand Charles HighamDepartment of Anthropology and Archaeology, University of Otago, North Dunedin, New Zealand Mark J. HudsonMt Fuji World Heritage Centre for Mountain Research, Shizuoka, Japan Museum of Natural and Environmental History, Shizuoka, Japan Hsiao-chun HungDepartment of Archaeology and Natural History, College of Asia and the Pacific, The Australian National University, Canberra, Australia Michiko IntohDepartment of Social Research, National Museum of Ethnology, Osaka, Japan Timothy A. JinamDivision of Population Genetics, National Institute of Genetics, Shizuoka, Japan Hideaki Kanzawa-KiriyamaDepartment of Anthropology, National Museum of Nature and Science, Tokyo, Japan Nguyen Kim DungThe Vietnamese Institute of Archaeology, Hanoi, Vietnam Nguyen Lan CuongThe Vietnamese Institute of Archaeology, Hanoi, Vietnam Tracey L.-D. LuDepartment of Anthropology, the Chinese University of Hong Kong, Hong Kong, China Hirofumi MatsumuraFaculty of Health Science, Sapporo Medical University, Sapporo, Japan Armand Salvador MijaresArchaeological Studies Program, University of the Philippines, Quezon City, Philippines Carmen SarjeantSchool of Archaeology and Anthropology, College of Arts and Social Sciences, The Australian National University, Canberra, Australia Ken-ichi ShinodaDepartment of Anthropology, National Museum of Nature and Science, Tsukuba, Japan Tr...

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Genetic structure in village dogs reveals a Central Asian domestication origin

Cited by 186 publications

References 49 publications

Bottlenecks and selective sweeps during domestication have increased deleterious genetic variation in dogs

Bottlenecks and selective sweeps during domestication have increased deleterious genetic variation in dogs

On the origin of mongrels: evolutionary history of free-breeding dogs in Eurasia

New Perspectives in Southeast Asian and Pacific Prehistory

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