Genomic Analyses Reveal the Influence of Geographic Origin, Migration, and Hybridization on Modern Dog Breed Development - PubMed (original) (raw)

Genomic Analyses Reveal the Influence of Geographic Origin, Migration, and Hybridization on Modern Dog Breed Development

Heidi G Parker et al. Cell Rep. 2017.

Abstract

There are nearly 400 modern domestic dog breeds with a unique histories and genetic profiles. To track the genetic signatures of breed development, we have assembled the most diverse dataset of dog breeds, reflecting their extensive phenotypic variation and heritage. Combining genetic distance, migration, and genome-wide haplotype sharing analyses, we uncover geographic patterns of development and independent origins of common traits. Our analyses reveal the hybrid history of breeds and elucidate the effects of immigration, revealing for the first time a suggestion of New World dog within some modern breeds. Finally, we used cladistics and haplotype sharing to show that some common traits have arisen more than once in the history of the dog. These analyses characterize the complexities of breed development, resolving longstanding questions regarding individual breed origination, the effect of migration on geographically distinct breeds, and, by inference, transfer of trait and disease alleles among dog breeds.

Keywords: admixture; behavior; canine; domestication; migration; morphology; population.

Copyright © 2017 The Author(s). Published by Elsevier Inc. All rights reserved.

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Figures

Figure 1

Figure 1

Cladogram of 161 domestic dog breeds. Breeds that form unique clades supported by 100% of bootstraps are combined into triangles. For all other branches the gold star =90% or better, Black star = 70% -89%, Silver star = 50% -69% bootstrap support. Breeds are listed on the perimeter of the circle. A small number of dogs do not cluster with the rest of their breed indicated as follows: * - Cane paratore; + - Peruvian Hairless dog; # - Sloughi; @ - Country of origin Salukis; ^ - Miniature Xoloitzcuintli

Figure 2

Figure 2

Representatives from each of the 23 clades of breeds. Breeds and clades are listed for each picture from left to right, top to bottom: a)Akita – Asian Spitz, b) Shih Tzu – Asian Toy (by Mary Bloom), c) Icelandic sheepdog – Nordic Spitz (by Veronica Druk) d) Miniature Schnauzer - Schnauzer, e) Pomeranian – Small Spitz, f) Brussels Griffon – Toy Spitz (by Mary Bloom), g) Puli - Hungarian, h) Standard Poodle - Poodle, i) Chihuahua – American Toy, j) Rat Terrier – American Terrier (by Stacy Zimmerman), k) Miniature Pinscher - Pinscher, l) Irish Terrier -Terrier, m) German Shepherd Dog - New World (by Mary Bloom), n) Saluki -Mediterranean (by Mary bloom), o) Basset Hound – Scent Hound (by Mary Bloom), p) American Cocker Spaniel – Spaniel (by Mary Bloom), q) Golden Retriever – Retriever (by Mary Bloom), r) German Shorthaired Pointer – Pointer Setter (by Mary Bloom), s)Briard – Continental Herder (by Mary Bloom), t)Shetland Sheepdog – U.K. Rural, u) Rottweiler - Drover, v) Saint Bernard - Alpine, w) English Mastiff – European Mastiff (by Mary Bloom).

Figure 3

Figure 3

Gross haplotype sharing across breeds. A) Boxplot of total haplotype sharing between all pairs of dogs from breeds within the same clade, across different clades and within the same breed. The difference between the distributions is highly significant, p<2e-16. B) Example of haplotype sharing between three breeds (Samoyed, Chow Chow and Keeshond) and a fourth (Eurasier) that was created as a composite of the other three. Combined haplotype length is displayed on the y-axis, 169 breeds and populations are listed on the x-axis in the order they appear on the cladogram starting with the jackal and continuing counter-clockwise. Haplotype sharing of zero is set at 250,000 for graphing, a value just below what is detected in this analysis. Breeds are colored by clade. 95% significance level is indicated by the horizontal line. Breed abbreviations are listed under the graph, in the order they appear and colored by clade.

Figure 4

Figure 4

Haplotype sharing between breeds from different phylogenetic clades. The circos plot is ordered and colored to match the tree in Figure 1. Ribbons connecting breeds indicate a median haplotype sharing between all dogs of each breed in excess of 95% of all haplotype sharing across clades.

Figure 5

Figure 5

Total haplotype sharing is inversely correlated with the time of hybridization between breeds that have developed within the last 200 years. A) The time of hybridization in years-before-present is graphed on the X-axis and the median total haplotype sharing on the Y-axis for six breeds of dog with reliable recent histories of admixture in breed formation or recovery. The trendline shows a linear correlation with r2=1. B) The slope and intercept of the trendline from A was applied to the median haplotype sharing values from the data for four additional breeds with reliable breed creation dates to establish accuracy of estimated hybridization dates.

Figure 6

Figure 6

Assessment of migration between breeds within clades. Admixture was measured in Treemix for 18 groups of breeds representing clades or combinations of small clades. A) Improvement to the maximum likelihood tree of each group as the result of admixture. They-axis shows fold improvement over the zero admixture tree. B) Cladogram of the New World breeds with European herders allowing four migration events. Arrows show estimated migration between breeds colored by weight (yellow to red = 0 - 0.5). C) Cladogram showing migration within the Asian Toy clade including a neighboring breed, the Tibetan Terrier. Pictures by Yuri Hooker (INCA), Mary Bloom (GSD and SHIH), Maurizio Marziali (CPAT), Mary Malkiel (COOK) and John & Debbie Caponetto (large and small XOLO/MXOL)

Figure 7

Figure 7

Haplotypes shared with breeds that carry known deleterious mutations. Breeds are connected if the median shared haplotype size exceeds the 95% threshold for interclade sharing. Sharing between breeds that are known to carry the mutation are colored black, sharing with other breeds are colored according to the breed that carries the mutation. A) Collie eye anomaly is found in a number of herding breeds developed in the UK and some sporting breeds developed in the US. B) Multi-drug resistance 1 mutation is carried by many UK herding breeds as well as the German Shepherd.

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