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Analysis of the origin and spread of the domestic dog using Y-chromosome DNA and mtDNA sequence data
KTH, School of Biotechnology (BIO), Gene Technology. (Evolutionary genetics and forensics)
2012 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The domestic dog was probably the first domesticated animal, and the only one to spread to all continents in ancient times. The dog is one of the most phenotypically diverse animals, a result of human selection throughout dog history. Studies of the genetic origins and early spread of domestic dogs is important to gather information about biological and cultural mechanisms behind domestication but also to investigate early human history. The step from a hunter and gatherer lifestyle to farming is one of the most important steps in human history. In this thesis I will present work aimed at understanding both domestic dog origins and dispersal. In order to be able to investigate dog origins based on a second haploid chromosome we identified 14,437 bp of Y-chromosomal DNA sequence. Based on this we show that dogs in Asia south of Yangtze River (ASY) has the highest genetic diversity and was founded from a large number of wolf founders confirming earlier mtDNA results. Early dog dispersal is tightly coupled to human history with the dog brought along as a cultural item. We have for the first time investigated the dog dispersal into Polynesia and Australia and our data can be used as evidence for a more complex settlement of Polynesia than earlier indicated from archaeological and linguistic studies. Analysis of Y-chromosome SNPs in Australian dingoes confirms earlier mtDNA genetic studies that the dingo is part of the domestic dog phylogeny and was founded from a small population of domestic dogs. We have also for the first time investigated the dog population on Madagascar and our data strongly indicates a mainland African origin for the Madagascan dogs. Finally, we have investigated the American dog population sampled from throughout the continent and also for the first time included putative indigenous breed dogs such as Chihuahua and Pero Sín Pelo del Peru, and the free-ranging Carolina dogs from southern USA. Our data clearly indicates a primarily Old World origin for the indigenous breed dogs and also for the free-ranging Carolina dogs in USA. We can also for the first time present evidence for continuity between the ancient and extant dog population with e.g. exclusive sharing of a haplotype between a modern sample of Chihuahua and an ancient Mexican sample.

Place, publisher, year, edition, pages
Stockholm: KTH Royal Institute of Technology, 2012. , 66 p.
Series
Trita-BIO-Report, ISSN 1654-2312 ; 2012:6
Keyword [en]
mtDNA, domestication, Y-chromosome, SNP, ASY, dog, dingo
National Category
Other Industrial Biotechnology
Identifiers
URN: urn:nbn:se:kth:diva-94145ISBN: 978-91-7501-364-0 (print)OAI: oai:DiVA.org:kth-94145DiVA: diva2:525521
Public defence
2012-05-25, Lennart Nilsson-salen, Nobels väg 15A, Solna, 13:00 (English)
Opponent
Supervisors
Funder
Swedish Research Council
Note
QC 20120510Available from: 2012-05-10 Created: 2012-05-08 Last updated: 2012-05-10Bibliographically approved
List of papers
1. Dog Y chromosomal DNA sequence: identification, sequencing and SNP discovery
Open this publication in new window or tab >>Dog Y chromosomal DNA sequence: identification, sequencing and SNP discovery
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2006 (English)In: BMC Genetics, ISSN 1471-2156, E-ISSN 1471-2156, Vol. 7Article in journal (Refereed) Published
Abstract [en]

Background: Population genetic studies of dogs have so far mainly been based on analysis of mitochondrial DNA, describing only the history of female dogs. To get a picture of the male history, as well as a second independent marker, there is a need for studies of biallelic Y-chromosome polymorphisms. However, there are no biallelic polymorphisms reported, and only 3200 bp of non-repetitive dog Y-chromosome sequence deposited in GenBank, necessitating the identification of dog Y chromosome sequence and the search for polymorphisms therein. The genome has been only partially sequenced for one male dog, disallowing mapping of the sequence into specific chromosomes. However, by comparing the male genome sequence to the complete female dog genome sequence, candidate Y-chromosome sequence may be identified by exclusion. Results: The male dog genome sequence was analysed by Blast search against the human genome to identify sequences with a best match to the human Y chromosome and to the female dog genome to identify those absent in the female genome. Candidate sequences were then tested for male specificity by PCR of five male and five female dogs. 32 sequences from the male genome, with a total length of 24 kbp, were identified as male specific, based on a match to the human Y chromosome, absence in the female dog genome and male specific PCR results. 14437 bp were then sequenced for 10 male dogs originating from Europe, Southwest Asia, Siberia, East Asia, Africa and America. Nine haplotypes were found, which were defined by 14 substitutions. The genetic distance between the haplotypes indicates that they originate from at least five wolf haplotypes. There was no obvious trend in the geographic distribution of the haplotypes. Conclusion: We have identified 24159 bp of dog Y-chromosome sequence to be used for population genetic studies. We sequenced 14437 bp in a worldwide collection of dogs, identifying 14 SNPs for future SNP analyses, and giving a first description of the dog Y-chromosome phylogeny.

Keyword
genome sequence, domestic dog, origin
National Category
Medical Biotechnology
Identifiers
urn:nbn:se:kth:diva-16107 (URN)10.1186/1471-2156-7-45 (DOI)000241743700001 ()2-s2.0-33750703200 (Scopus ID)
Note
QC 20100525Available from: 2010-08-05 Created: 2010-08-05 Last updated: 2017-12-12Bibliographically approved
2. Origins of domestic dog in Southern East Asia is supported by analysis of Y-chromosome DNA
Open this publication in new window or tab >>Origins of domestic dog in Southern East Asia is supported by analysis of Y-chromosome DNA
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2012 (English)In: Heredity, ISSN 0018-067X, E-ISSN 1365-2540, Vol. 108, no 5, 507-514 p.Article in journal (Refereed) Published
Abstract [en]

Global mitochondrial DNA (mtDNA) data indicates that the dog originates from domestication of wolf in Asia South of Yangtze River (ASY), with minor genetic contributions from dog-wolf hybridisation elsewhere. Archaeological data and autosomal single nucleotide polymorphism data have instead suggested that dogs originate from Europe and/or South West Asia but, because these datasets lack data from ASY, evidence pointing to ASY may have been overlooked. Analyses of additional markers for global datasets, including ASY, are therefore necessary to test if mtDNA phylogeography reflects the actual dog history and not merely stochastic events or selection. Here, we analyse 14 437 bp of Y-chromosome DNA sequence in 151 dogs sampled worldwide. We found 28 haplotypes distributed in five haplogroups. Two haplogroups were universally shared and included three haplotypes carried by 46% of all dogs, but two other haplogroups were primarily restricted to East Asia. Highest genetic diversity and virtually complete phylogenetic coverage was found within ASY. The 151 dogs were estimated to originate from 13-24 wolf founders, but there was no indication of post-domestication dog-wolf hybridisations. Thus, Y-chromosome and mtDNA data give strikingly similar pictures of dog phylogeography, most importantly that roughly 50% of the gene pools are shared universally but only ASY has nearly the full range of genetic diversity, such that the gene pools in all other regions may derive from ASY. This corroborates that ASY was the principal, and possibly sole region of wolf domestication, that a large number of wolves were domesticated, and that subsequent dog-wolf hybridisation contributed modestly to the dog gene pool.

Place, publisher, year, edition, pages
The Genetics Society, 2012
Keyword
dog, canis familiaris, domestication, Y-chromosome DNA, genetic diversity, phylogeography
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:kth:diva-49715 (URN)10.1038/hdy.2011.114 (DOI)000303001600008 ()22108628 (PubMedID)2-s2.0-84860013652 (Scopus ID)
Funder
Science for Life Laboratory - a national resource center for high-throughput molecular bioscienceSwedish Research CouncilKnut and Alice Wallenberg Foundation
Note
QC 20120509Available from: 2011-11-29 Created: 2011-11-29 Last updated: 2017-12-08Bibliographically approved
3. Mitochondrial DNA data indicate an introduction through Mainland Southeast Asia for Australian dingoes and Polynesian domestic dogs
Open this publication in new window or tab >>Mitochondrial DNA data indicate an introduction through Mainland Southeast Asia for Australian dingoes and Polynesian domestic dogs
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2012 (English)In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 279, no 1730, 967-974 p.Article in journal (Refereed) Published
Abstract [en]

In the late stages of the global dispersal of dogs, dingoes appear in the Australian archaeological record 3500 years BP, and dogs were one of three domesticates brought with the colonization of Polynesia, but the introduction routes to this region remain unknown. This also relates to questions about human history, such as to what extent the Polynesian culture was introduced with the Austronesian expansion from Taiwan or adopted en route, and whether pre-Neolithic Australia was culturally influenced by the surrounding Neolithic world. We investigate these questions by mapping the distribution of the mtDNA founder haplotypes for dingoes (A29) and ancient Polynesian dogs (Arc1 and Arc2) in samples across Southern East Asia (n = 424) and Island Southeast Asia (n = 219). All three haplotypes were found in South China, Mainland Southeast Asia and Indonesia but absent in Taiwan and the Philippines, and the mtDNA diversity among dingoes indicates an introduction to Australia 4600-18 300 years BP. These results suggest that Australian dingoes and Polynesian dogs originate from dogs introduced to Indonesia via Mainland Southeast Asia before the Neolithic, and not from Taiwan together with the Austronesian expansion. This underscores the complex origins of Polynesian culture and the isolation from Neolithic influence of the pre-Neolithic Australian culture.

Place, publisher, year, edition, pages
The Royal Society, 2012
Keyword
mitochondrial DNA, dingo, Polynesia, Australia, dog, haplotype
National Category
Developmental Biology
Identifiers
urn:nbn:se:kth:diva-90894 (URN)10.1098/rspb.2011.1395 (DOI)000299910400018 ()2-s2.0-84856256905 (Scopus ID)
Funder
Science for Life Laboratory - a national resource center for high-throughput molecular bioscience
Note
QC 20120307Available from: 2012-03-07 Created: 2012-03-05 Last updated: 2017-12-07Bibliographically approved
4. Narrow genetic basis for the Australian dingo confirmed through analysis of paternal ancestry
Open this publication in new window or tab >>Narrow genetic basis for the Australian dingo confirmed through analysis of paternal ancestry
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2012 (English)In: Genetica, ISSN 0016-6707, E-ISSN 1573-6857, Vol. 140, no 1-3, 65-73 p.Article in journal (Refereed) Published
Abstract [en]

The dingo (Canis lupus dingo) is an iconic animal in the native culture of Australia, but archaeological and molecular records indicate a relatively recent history on the continent. Studies of mitochondrial DNA (mtDNA) imply that the current dingo population was founded by a small population of already tamed dogs from Southeast Asia. However, the maternal genetic data might give a unilateral picture, and the gene pool has yet to be screened for paternal ancestry. We sequenced 14,437 bp of the Y-chromosome (Y-chr) from two dingoes and one New Guinea Singing Dog (NGSD). This positioned dingo and NGSD within the domestic dog Y-chr phylogeny, and produced one haplotype not detected before. With this data, we characterized 47 male dingoes in 30 Y-chr single-nucleotide polymorphism sites using protease-mediated allele-specific extension technology. Only two haplotypes, H3 and H60, were found among the dingoes, at frequencies of 68.1 and 31.9 %, respectively, compared to 27 haplotypes previously established in the domestic dog. While H3 is common among Southeast Asian dogs, H60 was specifically found in dingoes and the NGSD, but was related to Southeast Asian dog Y-chr haplotypes. H3 and H60 were observed exclusively in the western and eastern parts of Australia, respectively, but had a common range in Southeast. Thus, the Y-chr diversity was very low, similar to previous observations for d-loop mtDNA. Overall genetic evidence suggests a very restricted introduction of the first dingoes into Australia, possibly from New Guinea. This study further confirms the dingo as an isolated feral dog.

Keyword
Dingo, Canis familiaris, New Guinea Singing Dog, Y-chromosome, Single Nucleotide Polymorphism (SNP), Protease-mediated Allele-specific Extension (PrASE), Short Interspersed Element (SINE)
National Category
Biological Sciences
Identifiers
urn:nbn:se:kth:diva-94527 (URN)10.1007/s10709-012-9658-5 (DOI)000305886800006 ()2-s2.0-84863336209 (Scopus ID)
Funder
Swedish Research CouncilKnut and Alice Wallenberg FoundationScience for Life Laboratory - a national resource center for high-throughput molecular bioscience
Note

QC 20120730

Available from: 2012-05-10 Created: 2012-05-09 Last updated: 2017-12-07Bibliographically approved
5. African origin for Madagascan dogs revealed by mtDNA analysis
Open this publication in new window or tab >>African origin for Madagascan dogs revealed by mtDNA analysis
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Dogs were the only domestic animals accompanying humans to every continent in ancient time, and was along with pig and chicken part of the Austronesian Neolithic culture. Madagascar was one of the last major land masses to be occupied by humans, 1,500-2,000 years ago. It was initially colonized by Austronesian speaking Indonesians but subsequent migration from Africa has resulted in approximately equal genetic contribution from Indonesia and Africa, and the material culture has mainly African influences. To track the initial worldwide dispersal of dogs and illuminate this part of Madagascan cultural origins we here investigate the ancestry of Malagasy dogs. We analysed mtDNA control region sequences in dogs from Madagascar (n=145) and compared with dogs from potential ancestral populations in Island Southeast Asia (n=219) and sub-Saharan Africa (n=493). We found that 90% of the Madagascan dogs carried a haplotype present also in sub-Saharan Africa, and the remaining lineages could all be attributed to a likely origin in Africa. In contrast, only 26% of Malagasy dogs shared a haplotype with Indonesian dogs, all of which universally occurring haplotypes, and three haplotypes typical for Austronesian dogs, carried by >50% of Indonesian and Polynesian dogs, were carried by only 1% of the Madagscan dogs. Thus, in contrast to the human population, the Madagscan dogs seem to trace its origin entirely from Africa. This indicates that dogs were not brought with the initial Austronesian speaking colonizers on their trans-ocean voyage but introduced at a later stage with the migration and cultural influence from Africa.

National Category
Biological Sciences
Identifiers
urn:nbn:se:kth:diva-94475 (URN)
Note
QS 2012Available from: 2012-05-09 Created: 2012-05-09 Last updated: 2012-05-29Bibliographically approved
6. MtDNA analysis confirms early Pre‐Colombian origins of Native Americandogs
Open this publication in new window or tab >>MtDNA analysis confirms early Pre‐Colombian origins of Native Americandogs
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Dogs were present in Pre‐Columbian America, presumably brought to the New World by early human migrants of Asian origin. However, the extent to which historical Arctic, North and South American breeds, e.g. the Alaskan Malamute, Inuit, Eskimo and Greenland dogs, Xoloitzcuintli, Chihuahua and Perro Sín Pelo del Peru, are descendants of these original dogs or were replaced by European dogs remains to be assessed. Using a comprehensive phylogeographic analysis to trace the origin of their mitochondrial (mt) DNA lineages, these breeds were analysed for 582 bp of the mtDNA control region and compared to extensive samples of East Asian (n = 984) and European dogs (n = 639), and previously published Pre‐Columbian sequences. Evidence for a Pre‐Columbian origin was found for all putative American breeds based on the detection of haplotypes phylogenetically distinct from European haplotypes, exclusive to America, shared only with East Asia, or identical to ancient American sequences. Identical rare haplotypes in ancient and modern samples showed geographic continuity over time in Mexico (Chihuahua) and Alaska (Alaskan Malamute). A European origin for at most 15% of the female lineages was indicated, suggesting marginal replacement by European dogs. We also analysed free‐ranging dogs from the USA and South America. In agreement with a previous study, free ranging dogs in general showed little pre‐Columbian ancestry. However, for several populations an appreciable proportion of indigenous ancestry was indicated. Specifically, we provide the first DNA‐based evidence for an ancient Asian origin of the Carolina Dog, a dingo‐like free‐ranging population in the USA. Numerous dogs were probably brought from Asia, since totally 13 mtDNA haplotypes among extant and ancient American dogs were distinct from haploypes found in Europe.

Keyword
Dog, mitochondrial DNA, mtDNA, America, Pre‐Columbian
National Category
Biological Sciences
Identifiers
urn:nbn:se:kth:diva-94424 (URN)
Note
QS 2012Available from: 2012-05-09 Created: 2012-05-09 Last updated: 2012-05-10Bibliographically approved

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