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- Sprache: Englisch
The domestication of plants, animals and microorganisms has enabled the development of agriculture, animal husbandry, the processing of their products and, ultimately, civilizations.
The species concerned by domestication, the regions of the world where it could take place, the clues that enable us to identify wild ancestors, the particularly morphological or physiological properties that characterize it, the modified genes, the genetic exchanges that domesticated organisms maintained with their wild ancestors, and the consequences of the structuring of the species that resulted in animal breeds or plant varieties, are all questions that develop studies in the fields of archaeology, sociology, ecology and genetics.
Genetics of Domestications deals with the contribution of modern methods of genetic analysis and genomics to historical knowledge of domestications, their nature and diversity, based on examples of twelve species or groups of species.
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Table of Contents
Cover
Table of Contents
Title Page
Copyright Page
Introduction
1 Thousands of Years of Relationship between Man and Dog Revealed by Genomics
1.1. The history of dog domestication, the subject of much debate
1.2. Paleogenomics: an essential tool for understanding the evolutionary history of the dog
1.3. From commensalism to modern breeds: identifying the genomic foundations behind the intensification of the human–dog relationship
1.4. Selection of modern breeds, evolution in an anthropic context
1.5. References
2 Imprints of Domestication in the Sheep Genome
2.1. The cradle of domestication in the Middle East
2.2. Conquering the West
2.3. Africa
2.4. Asia
2.5. Conclusion
2.6. References
3 Humans and Pigs: Over Ten Thousand Years of Shared Evolution
3.1. The evolution of
Sus scrofa
over the last 2 million years
3.2. The genomics of adaptation in
Sus scrofa
3.3. The processes of pig domestication
3.4. Using archaeology and genomics to trace the history of pig domestication
3.5. The 19th century and the advent of the out stud-book
3.6. Before domestication: human-initiated movements of wild and domesticated pigs
3.7. Conclusion
3.8. References
4 The Domestication of the Wild Rabbit: Genetic and Genomic Elements
4.1. Phylogenetic context of the species
4.2. Origin and spread of the wild rabbit
4.3. A recent domestication
4.4. Back to the wild: an invasive species
4.5. Conclusion
4.6. References
5 Domesticated Poultry: A History Illuminated by Genomics
5.1. Introduction
5.2. Domestic birds and their phylogenetic context
5.3. Domestication scenarios
5.4. Genetic mechanisms involved in domestication
5.5. Conclusion
5.6. References
6 Genetics of Fish Domestication in Aquaculture
6.1. Introduction
6.2. Diverse, complex and poorly understood domestication histories
6.3. Significant performance improvements for domesticated species
6.4. A success story: Atlantic salmon
6.5. Conclusion
6.6. References
7 The Domestication of Yeast
7.1. The history of fermented products and the domestication of microorganisms
7.2. Yeast diversity and the evolutionary origins of fermentation
7.3. Population structure of yeast isolated from anthropic niches
7.4. Genetic basis for the evolutionary history of domesticated populations
7.5. Conclusion
7.6. References
8 The Domestication of
Oenococcus oeni
: A Bacterium Crafted for Wine Production
8.1. Introduction
8.2.
Oenococcus oeni
, a wine bacterium for MLF
8.3. Genetic characteristics of
O. oeni
domestication
8.4. Conclusion
8.5. References
9 Tracing the Origins of Wheat Cultivation
9.1. The different types of wheat, one of the most widely consumed cereals in the world
9.2. A species with ancient origins resulting from multiple hybridizations
9.3. Archaeological evidence of its origins: archaeobotany
9.4. Genetic evidence of wheat origins: paleogenomics
9.5. Perspectives: studying the origins and spread of wheat cultivation to support the selection of modern varieties
9.6. Acknowledgments
9.7. References
10 A History of Cultivated Rice Genomics
10.1. The history of rice: wild rice and cultivated rice
10.2. The beginnings of genomics and the pan-genomic revolution
10.3. Genomics’ contribution to the study of rice domestication
10.4. Conclusion: the “continuity” of domestication
10.5. References
11 Grapevine Domestication and Selection
11.1. Introduction
11.2.
Vitis vinifera L.
, the main species of the genus
Vitis
used for the production of table grapes and wine
11.3. Origin and domestication of
Vitis vinifera L.
11.4. The main traits that evolved during grapevine domestication
11.5. From domestication to the present day
11.6. The grapevine of tomorrow
11.7. References
12 Tomato Domestication and Breeding: A Major Contribution from Wild Species
12.1. Introduction
12.2. Origin of the cultivated tomato: wild ancestors and centers of domestication
12.3. The origins of cultivated tomatoes: genetic data
12.4. Post-domestication of the tomato after global expansion
12.5. Conclusion
12.6. References
13 Mutagenesis and Accelerated Domestication
13.1. Random mutagenesis and neo-domestication
13.2. Genome editing and domestication
13.3. Limits and constraints of neo-domestication
13.4. Conclusion
13.5. References
Glossary
List of Authors
Index
End User License Agreement
List of Tables
Chapter 5
Table 5.1. Status of genome data for major domesticated bird species. The pref...
Table 5.2. List of genes potentially associated with domestication, relating t...
Table 5.3. List of genes potentially associated with domestication, relating t...
Table 5.4. List of genes potentially associated with domestication and associa...
Table 5.5. List of genes potentially associated with domestication in relation...
Chapter 6
Table 6.1. Ranking of the 10 species whose production exceeded 1 million tons ...
Chapter 8
Table 8.1. Distribution of major exopolysaccharide production genes and gene c...
Chapter 11
Table 11.1. The main traits impacted by domestication and related to productio...
Chapter 12
Table 12.1. Main characteristics of species in the Lycopersicon section of the...
List of Illustrations
Chapter 1
Figure 1.1. Taymir wolf mandible fragment
Figure 1.2. Schematic representation of the chronology of human societal chang...
Figure 1.3. Dog population movements in Europe between the Paleolithicera and ...
Figure 1.4. Multiple dog introductions in North America (BP: before present)
Chapter 2
Figure 2.1. Phylogeny representing the relationships between three species of ...
Figure 2.2. Locating the initial domestication range of sheep by studying the ...
Figure 2.3. Genomic regions under selection overlapping the KITLG gene
Figure 2.4. Main sheep diffusion routes in Europe
Figure 2.5. Location of sheep populations with primitive retrotypes, according...
Figure 2.6. Fat-tailed sheep depicted by Job Ludolphus in A New History of Eth...
Figure 2.7. Main sheep diffusion routes in Africa
Figure 2.8. Main sheep diffusion routes in Asia
Chapter 3
Figure 3.1. Geographical range and phylogenetic relationships of Sus species
Figure 3.2. Map showing the ancestry of former domesticated pigs and wild boar...
Chapter 4
Figure 4.1. Simplified phylogeny illustrating the families and genera of nonex...
Figure 4.2. Example of the geographical distribution of A and B lineages in th...
Chapter 5
Figure 5.1. Phylogeny of birds. The length of the branches indicates the diverge...
Figure 5.2. Most probable topologies of phylogenetic relationships between pre...
Figure 5.3. Diagram of divergent lines and Advanced InterCrosses (AIC).
Chapter 6
Figure 6.1. Evolution of an animal species during the domestication process: 1...
Figure 6.2. Lifecycle of a fish, taking the perch as an example (Perca fluviat...
Figure 6.3. Number of species by level of domestication (in 2009)
Figure 6.4. Global Atlantic salmon production from 1950 to 2016
Chapter 7
Figure 7.1. Microorganism domestication continuum
Figure 7.2. Diversity and specialization of yeast species in four fermented fo...
Figure 7.3. Common Saccharomyces hybrids with their isolation medium Saccharomy...
Figure 7.4. Genomics of domestication in Saccharomyces cerevisiae. Functions o...
Chapter 8
Figure 8.1. Key stages in the description of O. oeni and MLF
Figure 8.2. (a) Phylogenetic distribution of 226 O. oeni strains in four major...
Figure 8.3. Chromosomal localization of genes and gene clusters associated wit...
Chapter 9
Figure 9.1. Global distribution of wheat production in 2019, expressed in tons...
Figure 9.2. Evolutionary model of modern wheat.
Figure 9.3. Spike morphology in wild and domesticated wheat
Figure 9.4. Origins and expansion of agriculture in Europe.
Chapter 10
Figure 10.1. Diagram illustrating the concepts of pan-genome, core genome and ...
Chapter 11
Figure 11.1. Presentation of the vine’s taxonomic position
Figure 11.2. Morphological diversity of some Vitis species, in collections or ...
Figure 11.3. Example of diversity in berry shape and color in Vitis sylvestris...
Figure 11.4. Example of generation overlap: Dattier de Beyrouth, which is a pa...
Chapter 12
Figure 12.1. Shape and color diversity of tomato varieties
Figure 12.2. Relationship between the diversity of wild forms and cherry tomat...
Figure 12.3. Representation of the diversity of 1,000 tomato accessions of S. ...
Figure 12.4. Diagram of the appearance of fruit shape mutations from the wild ...
Figure 12.5. Evolution of tomato domestication from S. pimpinellifolium (SP) t...
Figure 12.6. An early depiction of a tomato plant
Chapter 13
Figure 13.1. Illustration of the molecular scissors (CRISPR Cas9), which cuts ...
Figure 13.2. Physalis pruinosa.
Figure 13.3. Allotetraploid wild rice Oryza alta (a) and a line with a more co...
Guide
Cover Page
Table of Contents
Title Page
Copyright Page
Introduction
Begin Reading
Glossary
List of Authors
Index
WILEY END USER LICENSE AGREEMENT
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SCIENCES
Biology, Field Director – Marie-Christine Maurel
Genetics, Epigenetics, Subject Head – Bernard Dujon
Genetics of Domestications
Coordinated by
Georges Pelletier
First published 2024 in Great Britain and the United States by ISTE Ltd and John Wiley & Sons, Inc.
Apart from any fair dealing for the purposes of research or private study, or criticism or review, as permitted under the Copyright, Designs and Patents Act 1988, this publication may only be reproduced, stored or transmitted, in any form or by any means, with the prior permission in writing of the publishers, or in the case of reprographic reproduction in accordance with the terms and licenses issued by the CLA. Enquiries concerning reproduction outside these terms should be sent to the publishers at the undermentioned address:
ISTE Ltd27-37 St George’s RoadLondon SW19 4EUUK
www.iste.co.uk
John Wiley & Sons, Inc.111 River StreetHoboken, NJ 07030USA
www.wiley.com
© ISTE Ltd 2024The rights of Georges Pelletier to be identified as the author of this work have been asserted by him in accordance with the Copyright, Designs and Patents Act 1988.
Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s), contributor(s) or editor(s) and do not necessarily reflect the views of ISTE Group.
Library of Congress Control Number: 2024935671
British Library Cataloguing-in-Publication DataA CIP record for this book is available from the British LibraryISBN 978-1-78945-167-2
ERC code:LS2 Genetics, ’Omics’, Bioinformatics and Systems Biology LS2_5 Epigenetics and gene regulationLS3 Cellular and Developmental Biology LS3_9 Developmental genetics in animals and plants
Introduction
Michèle TIXIER-BOICHARD1 and Georges PELLETIER2,3
1GABI, INRAE, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, France
2Académie des sciences, Paris, France
3Académie d’agriculture de France, Paris, France
Based on a definition
Domestic, in the first sense, means belonging to the house, in Latin “domus”. Thus, for a living being, it means living in a home, in the broadest sense, of man, being raised and fed there. The domestication of animals, plants and microorganisms is therefore a process of adapting individuals, then their descendants, to an environment that is modified by human groups. This adaptation is associated with hereditary transformations that are conducive to their exploitation, which are expressed, for example, in an animal’s docile nature or the limitation of the spontaneous dispersal of cereal grains. In some cases, the species disappears in the wild and is only represented by domesticated types. Domestication can thus be seen as evolutionary pressure. A generic definition of domestication has been proposed by the Convention on Biological Diversity1 as follows: “‘Domesticated or cultivated species’ means species in which the evolutionary process has been influenced by humans to meet their needs”.
The transition from the wild to the domesticated state is just a starting point, because as human needs continue to evolve, so does the adaptation and management of domesticated species. Domestication can thus be seen as a process of accumulating heritable modifications to the characteristics of a group of individuals, enabling them to better meet the needs of our species, not only for survival, but also for pleasure, or for cultural or symbolic reasons. These genetic transformations of the species we have chosen, and the history of their exploitation for a variety of needs, have led to a diversification of animal breeds and plant varieties, in addition to strains of microorganisms involved in the manufacture of many fermented foods, such as beer, wine, bread, cheese and more. The history of their domestication has become increasingly well documented since the advent of modern DNA analysis technologies, revealing a plethora of strains and species whose ability to evolve and exchange genes contributes to the quality of these products.
Understanding domestication
When and where did domestication begin? How did it happen?
The history of domestication is intimately linked to human history or, more accurately, to the history of different human groups scattered across the planet. Archaeological digs enable us to reconstruct the past of certain species by uncovering their remains and using all the technical resources of archaeobotany and archaeozoology,2 from morphological description to various types of analysis. These include, for example, carbon isotope content for dating, or DNA sequences that can be extracted to reveal their relationship with today’s domesticated species.
In terms of the evolution of modern man, whose emergence can be traced back some 300,000 years to Africa, before migrating to the Eurasian continent and later to Australia and the Americas, the first domestications only appeared very late, in the last two tens of thousands of years before us: dog, man’s oldest companion, is thought to have been domesticated for at least 25,000 years. Over the last 12,000 years, plant species have undergone new types of genetic selection, corresponding to the needs of populations and leading to the emergence of agricultural societies in various parts of the world (Purruganan and Fuller 2009). Up until then, man had already been using plant and animal resources through gathering and hunting. Thus, the use of selectively harvested wild cereals, which spontaneously seeded and invaded areas occupied by populations, shows a first stage of co-evolution between man and a species used to make food. Evidence of this can be found in the Paleolithic period, like the case of millet in northern China 28,000 years ago, or barley and wheat, with potential signs of cultivation 23,000 years ago by hunter-gatherers who set up sedentary sites in the Middle East. The beginnings of bread-making are confirmed to have started 14,600 years ago, well before the domestication of wheat. The satisfaction of these needs led to new economic activity involving work in the fields, and the storage and processing of harvests. The seasonal nature of cereals led to the construction of storage facilities. The granaries that precede the emergence of domestication by at least 1,000 years represent a critical change in the relationship between humans and plant foods, with new social organizations of sedentary communities and the emergence of agriculture (Willcox and Stordeur 2012; Vigne 2015).
Different species have been involved in different regions on all continents, identified as hotbeds of domestication. Examples include the Fertile Crescent in the Middle East (wheat, barley, lentils, peas, chickpeas, ruminants, pigeon, cat and cochineal), China and Southeast Asia (rice, millet, soy, pig, chicken and duck), sub-Saharan Africa (sorghum, rice, millet and faba bean), Mesoamerica (corn, bean, pumpkin and turkey) and the Andes (potato, bean, quinoa and llama). Domestication initiated in one region is generally followed by a migration phase, as human populations travel with their seeds and animals. For example, many plant species were consumed by hunter-gatherers in the Amazon basin. Once domesticated, these species were gradually spread to other regions of the world, following human migrations or, more recently, following the discovery of America, leading to the exploitation in Europe of sunflowers, squash, pumpkins, corn, manioc, taro, potatoes, tomatoes, sweet potatoes, beans, cotton plants and so on.
The motivations behind domestication are certainly diverse. The controlled availability of cereals (and legumes) that could be stored, as well as the possibility of cooking particular foods (wheat bread) or alcoholic beverages (fermented barley) could be, more than a quest for calories, determining factors in the choice of these two main cereals cultivated in the Middle East, whose characteristics are not found in other wild grasses. Participating in the provisioning of social feasts in a region where, at the outset, there was no evidence of demographic pressure, and where fruits and nuts were abundant, a growing cultural interest in these species would have been a determining factor. In the case of animals, three modalities have been proposed to describe domestication (Larson and Fuller 2014). The commensal pathway corresponds to the case of an animal species living in the vicinity of humans with mutual benefit and involves no human intention. The other two pathways involve human intention, with either the predatory pathway, motivated by the need to obtain supplementary food resources (as a possible reaction to over-hunting), or the directed pathway, for any other intention, such as transport or distraction. However, these three pathways are not mutually exclusive: it is likely that domestication first followed a commensal or predatory path before humans acquired the intention of influencing or modifying an animal species for their own benefit.
The processes of domestication and selection have created ever-closer links between agriculture and society, accompanied by changes in human society. Increased yields have made agricultural production systems more dependent on continuous investment in labor, leading to a form of servitude. The domestication of the horse had a major impact on the mobility of human populations, while that of cattle had a major impact on work capacity in the fields.
The genetics of domestication
Which species have been domesticated? How can we identify wild ancestors? What specific morphological or physiological properties characterize it? What genes and gene modifications are involved? Have domesticated organisms been particularly isolated or have they maintained genetic exchanges with their wild ancestor (Hunter 2018)?
Analysis of the phylogeny of animal and plant species does not show a random distribution of domesticated species. This is particularly clear in the case of animals, where it can be seen that domesticated mammals, known as “cash crops”, are derived from only a small fraction of the phylogenetic and phenotypic diversity of mammals, with an over-representation of the order Artiodactyla (Bovidae: cattle, goats, sheep; Suidae: pigs, etc.), and a few species from the orders Rodentia (guinea pig), Lagomorpha (rabbit) and Perissodactyla (horse, donkey). The other domestic species are essentially from the order Carnivora, phylogenetically close to Artiodactyla and Perissodactyla (in the Ferungulata group). Some authors have jointly analyzed the phylogenetic position and biological or ecological particularities of domesticated species, whether they be animal or plant, and have concluded that certain species are predisposed to others (Milla et al. 2018). The domestication of different cereals (wheat, barley, rice, corn, sorghum and millet), characterized by the loss of spontaneous grain dispersal and dormancy, as well as an increase in grain size, has given rise to the concept of a “domestication syndrome”: common characteristics based on a limited number of mutations, but not implying an identity of these mutations. This concept is only valid if we also accept that characteristics vary according to species type and use: the domestication of cabbage and turnip has led to many different types for the consumption of leaves, roots, stems, inflorescences or the production of edible oil, or for lighting.
Advances in molecular biology and bioinformatics have given us detailed knowledge of the genome that has revolutionized the answers to the questions above. In particular, the study of ancient DNA makes it possible to attribute traits to archaeological remains that do not appear through morphology or chemical composition, such as coat color or fecundity, when the corresponding genetic markers are available (Frantz et al. 2020; Przelomska et al. 2020). It is now possible to compare ancient and recent genomes from domesticated and wild individuals sampled in different parts of the world, in order to estimate the size of the population involved in the initial domestication process, to pinpoint the place or places where a species was domesticated, to identify the genes or chromosomal regions modified by this process, or to retrace the history of populations after domestication. A significant challenge is to be able to distinguish genetic variants that have been favored by domestication, from those that have evolved randomly as a result of genetic drift, or indeed from those whose frequency has changed in response to recent selection. In the wake of domestication, species have been structured into animal breeds or plant varieties, but they may still have exchanges with their wild ancestors. Genetic methods and, where possible, ancient DNA enable us to sort out all the exchanges that have taken place over time.
Domestication is therefore a fascinating process, which has given rise to research in the fields of archaeology, sociology, ecology and genetics. The aim of this book is to illustrate the contribution of the most modern methods of genetic and genomic analysis to our historical understanding of domestication and its biological nature and diversity, based on the examples of 12 species or groups of species from the animal, plant and microorganism worlds, discussed by world-renowned specialists.
References
Frantz, L.A., Bradley, D.G., Larson, G., Orlando, L. (2020). Animal domestication in the era of ancient genomics.
Nature Reviews Genetics
, 21(8), 449–460. doi: 10.1038/s41576-020-0225-0.
Hunter, P. (2018). The genetics of domestication.
EMBO Reports
, 19(2), 201–205. doi: 10.15252/embr.201745664.
Larson, G. and Fuller, D.Q. (2014). The evolution of animal domestication.
Annual Review of Ecology, Evolution, and Systematics
, 45, 115–136. doi: 10.1146/annurev-ecolsys-110512-135813.
Milla, R., Bastida, J.M., Turcotte, M.M., Jones, G., Violle, C., Osborne, C.P., Chacón-Labella, J., Sosinski, E.E., Jr., Kattge, J., Laughlin, D.C. et al. (2018). Phylogenetic patterns and phenotypic profiles of the species of plants and mammals farmed for food.
Nature Ecology & Evolution
, 2, 1808–1817. doi: 10.1038/s41559-018-0690-4.
Przelomska, N.A., Armstrong, C.G., Kistler, L. (2020). Ancient plant DNA as a window into the cultural heritage and biodiversity of our food system.
Frontiers in Ecology and Evolution
, 8, 74. doi: 10.3389/fevo.2020.00074.
Purugganan, M.D. and Fuller, D.Q. (2009). The nature of selection during plant domestication.
Nature
, 457(7231), 843–848. doi: 10.1038/nature07895.
Vigne, J.D. (2015). Early domestication and farming: What should we know or do for a better understanding.
Anthropozoologica
, 50(2), 123–150. doi: 10.5252/az2015n2a5.
Willcox, G. and Stordeur, D. (2012). Large-scale cereal processing before domestication during the tenth millennium cal BC in northern Syria.
Antiquity
, 86, 99–114 [Online]. Available at:
http://antiquity.ac.uk/ant/086/ant0860099.htm
.
Notes
1
Available at:
https://www.cbd.int/convention/
.
2
Analysis and interpretation of plant and animal remains found on archaeological sites.
1Thousands of Years of Relationship between Man and Dog Revealed by Genomics
Morgane OLLIVIER
ECOBIO, Université de Rennes, France
The dog was the first animal to be domesticated by humans, at least 25,000 years ago. Its domestication was made possible by the wide and abundant distribution of its wild ancestor, the wolf, in the northern hemisphere, where human societies were evolving at the end of the Paleolithic era. The wolf’s history is therefore atypical of other domesticated species, as its domestication began well before the Neolithic transition. It is not easy to pinpoint a precise date for domestication.
It is important to remember that domestication is a gradual process, and so the dog/wolf distinction is only possible when the characteristics of domestication are visible. The first dogs were probably morphologically very similar to wolves, and so cannot easily be distinguished from one another. Wolves also had a very wide distribution (the entire northern hemisphere), making it all the more difficult to classify remains solely on the basis of geography. Canid fossils are also rare, and consequently the archive is both temporally and geographically fragmented. In this chapter, we will review the main lines of research carried out over the last 20 years, which have shed light on the evolutionary history of the dog and its relationship with man.
1.1. The history of dog domestication, the subject of much debate
1.1.1. The dog: domesticated since the Paleolithic period
The appearance of dogs in the fossil record is recent, and current debates center on whether dogs first appeared in the late Paleolithic or early Neolithic periods. On archaeological grounds, the divergence between dog and wolf is thought to have occurred between 16,000 and 11,000 years BP, a time interval that corresponds to the age of the first undisputed ancient dog remains found in both Europe and Asia at numerous remote archaeological sites (Vigne 2005). Earlier dates have been proposed on the basis of remains initially assumed to be dogs. In Europe, these include remains from the sites of Předmostí in the Czech Republic, estimated at 27,000 years BP, and Goyet in Belgium, estimated at 36,000 years. In Asia, remains found in the Altai Mountains in Russia date back some 33,000 years. However, recent work has cast doubt on these conclusions, demonstrating that the morphology of the specimens studied was within the range of morphological variation of late Pleistocene wolves. For example, fossil Belgian canids, including the Goyet dog, form a sister group to all contemporary dogs and wolves, suggesting that they represent either a failed domestication event, or a morphologically distinct form of wolf.
In 2015, the genome of a 35,000-year-old wolf from the Taimyr Peninsula in northern Siberia was sequenced. By comparing this genome with that of the modern wolf and that of the present-day dog and based on an estimate of the mutation rate between these genomes, it was concluded that the ancestors of dogs were separated from present-day wolves before the Last Glacial Maximum and the Taymir wolf (Figure 1.1) belonged to a population that had already diverged from the common ancestor of modern wolves and dogs. Dogs are probably descended from extinct wolf populations that diverged from the ancestors of extant wolves around 27,000–40,000 years ago (Skoglund 2015). Present-day gray wolves would not be their direct ancestors, and it is likely that the modern-day dogs, which are closest to these wolves, are the result of multiple hybridizations (Frantz et al. 2016). The disappearance of these populations could be explained by the decline in wolf populations during the Last Glacial Maximum, which then led to the repopulation, expansion and replacement of ancestral populations by current populations. The wolf population from which dogs most likely descend were large northern wolves, and none of the current wolf lineages from the hypothetical regions of domestication appear to be the original source population (Skoglund et al. 2015). These studies therefore suggest that dogs probably originated in Eurasia as early as 33,000 years ago, an earlier date than their first record in the archaeological record, and that their evolutionary history is complex along a long phenotypic continuum.
Figure 1.1.Taymir wolf mandible fragment
(source: Reuters).
1.1.2. The process behind dog domestication
Domestication leads to the appropriation and control by a human society of an animal or plant sub-population for the production of a service or commodity. It involves an evolutionary process that documents two aspects of evolution: speciation and adaptation. In the domestication process, these two biological mechanisms consist, on the one hand, of a relative break in gene flow between the original population and the domesticated population and, on the other hand, of a modification in selective pressures. Based on ethnographic research suggesting that domestic animal husbandry was not unusual among hunter-gatherer groups worldwide, Francis Galton suggested that dogs had been domesticated following the capture and rearing of cubs in human camps. Later, Belyaev (1969) showed that animal domestication could have begun in the absence of deliberate human design and action. In 2011, Vigne (2011) proposed a multi-stage model characterized by a gradually intensifying relationship between humans and animals. In this perspective, animal domestication proceeded along a continuum from anthropophilia to commensalism, control in the wild, control of animals in captivity, extensive breeding, intensive breeding and, finally, pets. While Zeder (2012) has also acknowledged this model’s step-by-step approach, she describes three distinct paths that animals may have followed in a domestic relationship with humans: a commensal path, a prey path and a directed path.
Figure 1.2.Schematic representation of the chronology of human societal change and the history of the dog in Western Europe
(source: M. Ollivier).
In the case of the dog, it is assumed that the domestication process first took the form of commensalism/mutualism (Vigne 2011) between wolves and humans at the end of the Paleolithic era (Vigne 2005). The commensal pathway does not begin with intentional human action to bring wild animals (juvenile or otherwise) into their camps. Instead, different wild animal populations would have been attracted by elements of the human niche, including human food waste.
The individuals most able to take advantage of the resources associated with human camps would have been the more docile, less aggressive individuals. A recent study supported this view, proposing a hypothesis based on the sharing of resources between humans and wolves. Humans are not fully adapted to a carnivore diet, as their meat consumption is limited by the liver’s ability to remove the ammonia produced by protein digestion.
Unlike humans, wolves can thrive on lean meat for months on end. Yet the study shows that all Pleistocene archaeological sites where dog remains have been found originate from areas similar to subarctic and arctic environments. Calculations show that during harsh winters, when game was lean and lacking in fat, late Pleistocene hunter-gatherers in Eurasia would have benefited from a surplus of animal protein that could have been shared with early dogs. This study explains how competition may have contributed to the initial phase of domestication.
Thus, the relationship between man and dog probably involved a gradual taming of the wolf linked to a cultural process (Larson and Burger 2013), particularly in Europe, where it is likely that such interactions began over 30,000 years ago. After the first phase of domestication, dogs would have become more docile, being used in a multitude of ways, such as hunting companions, beasts of burden, guards, and would have undergone many evolutionary changes similar to those of humans.
1.1.3. The number and location of domestication events: contextualization and the contribution of archaeological and genomic data
Gray wolves were distributed throughout the northern hemisphere, and it is assumed that the wolf populations that gave rise to dogs, in whole or in part, are certainly extinct. Furthermore, the human populations that domesticated wolves were mobile hunter-gatherers. For these reasons, it has long been difficult to establish where dogs were domesticated, or even whether several wolf populations were domesticated independently. Several morphological groups can also be distinguished among Upper Paleolithic dogs: large, robust canids are observed in northeastern and central Europe, while medium-sized dogs with strong allometric differences are described in the Middle East. Lastly, small-sized individuals are found in southwestern Europe. This morphological diversity, as well as the temporal concordance of dog samples found in both Europe and Asia, with the wide distribution of wild ancestors and Upper Paleolithic dogs, has been interpreted by archaeozoologists since the 19th century as a strong argument for multiple, independent domestications.
Genetic studies of the diversity of today’s dog breeds, on the other hand, have led to contradictory and sometimes opposing conclusions. Analysis of the mitochondrial DNA of 162 wolves from 27 locations worldwide, and 140 domestic dogs representing 67 breeds, shows that most dog sequences belong to a single group in which no wolf sequences are found. However, in three other groups, both dog and wolf mitochondrial sequences are found, which the authors interpret as an initial domestication event, followed by repeated cycles of hybridization and selection for canine phenotypic variation. Repeated genetic exchanges between dog and wolf populations may have been a significant source of variation for artificial breed selection. Analysis of a 582-base-pair region of mitochondrial DNA from 654 domestic dogs from Europe, Asia, Africa and Arctic America, as well as 38 Eurasian wolves, shows that haplogroup A1 is dominant over the other five (B, C, D, E and F), and that dogs with a Southeast Asian origin show greater genetic diversity. This DNA region was also analyzed in 1543 Old World dogs, including modern breeds of known geographical origin, as well as breeding dogs of indigenous ancestry, which are more relevant for unravelling the origins of the dog than modern breeds. The results point in the same direction, showing greater genetic diversity in Asia, with Western Eurasian haplotypes all attributed to an East Asian haplotype. These studies thus proposed East Asia as the main and only center of domestication, based on comparisons of genetic diversity between regions, hypothesizing that centers of origin contain greater genetic variation. A new interpretation was subsequently given to this observation by some authors, who suggested that it reflected a replacement of native European canine ancestry by more recent lines of Southeast Asian immigrants. This replacement may have been accompanied by a general geographical expansion of East Asian dog populations or, alternatively, explained by human transportation in connection with trade.
Other studies, again based on modern DNA, suggest, on the contrary, and in line with archaeological evidence, that several centers of domestication existed in Eurasia. For example, mitochondrial DNA diversity in African village dogs is comparable to that of East Asian dogs. This discovery was used to question the Southeast Asian origin of the dogs. Subsequent analysis of 48,036 nuclear genome SNP positions in 912 modern dog breeds, 225 wolves and 60 coyotes, demonstrates that Middle Eastern wolves contribute a significant amount of genomic diversity to modern dog breeds, suggesting a Middle Eastern contribution to the history of dog domestication.
Various observations may explain why it is so difficult to unravel the origins of dogs from current genetic data: (i) most dog breeds have very recent origins, with a history going back less than 150 years; (ii) dog populations have undergone numerous episodes of diversification, hybridization and homogenization, reducing the resolving power of genetic data from modern breeds; (iii) a combination of introgressions and bottlenecks between dog and wolf populations, well after the domestication process, may have blurred modern genomic signatures and reduced our ability to make a distinction between the initial domestication process(es) and post-domestication gene flow; (iv) the wolf population(s) that gave rise to modern dogs may be extinct, making it difficult to detect the initial process using studies based on modern data. The paleogenomic approach therefore appears to be the most effective tool for tracing the history of dog domestication.
1.2. Paleogenomics: an essential tool for understanding the evolutionary history of the dog
Understanding the origins and early history of dogs has been complicated by bottlenecks, expansions, extinctions as well as local replacements and gene flows between wolves and dogs. Large-scale systematic research and analysis of ancient wolf and dog genomes across space and time is therefore needed to accurately reconstruct the evolutionary history of the first domestic animal.
1.2.1. Eurasian origins and diffusion
In 2013, the first mitochondrial genomes of ancient dogs and wolves were published and began to provide answers. The results show that dogs and wolves do not form two distinct monophyletic groups. Each of the clades grouping modern dogs of haplogroups A, C and D have an ancient lineage as a sister group, grouping ancient European dogs and wolves. It was thus demonstrated that dogs have a European origin and have been descended from a line of wolves for over 20,000 years, a line that is now extinct. Following this, the analysis of over 99 mitochondrial sequences of Upper Paleolithicto Bronze Age individuals from 29 archaeological sites in Eurasia, and the complete genome of the Newgrange dog (late Neolithic, ~ 4,800 ago) in Ireland suggested that dogs, in both Eastern and Western Eurasia, were independently domesticated in the Upper Paleolithic from several wolf populations (Frantz et al. 2016). Later, during the Neolithic and early Bronze Age, Asian dog lineages spread westwards, leading to a profound change in the European dog population (Ollivier et al. 2018). Two types of diffusion seem to have taken place: one linked to the Neolithic transition, which may have originated in the Middle East, and a later one from Asia to Europe at the end of the Neolithic/Chalcolithic period, probably via the Pontic steppes and accompanied by other elements such as millet, the domestic horse and early metallurgy. Thus, human movements and cultural diffusion have profoundly shaped the lineage of dogs. Lastly, a very recent study shows that this scenario could be even more complex. By sequencing 27 ancient dog genomes from across Eurasia, Bergström et al. (2020) confirm that all dogs derive from a lineage of wolves that are distinct from present-day wolves and also show, as suggested by archaeozoological data, that five major lineages were already present and diversified 11,000 years ago, as early as the Paleolithic period. The fate of each of these lineages is therefore linked to, and even mirrors, migrations and the history of human populations. By studying the evolutionary history of the dog, we can retrace the history of mankind.
Figure 1.3.Dog population movements in Europe between the Paleolithicera and the Bronze Age, inferred by mitochondrial data (Hg: haplogroup; BP: before present)
(source: adapted from Ollivier et al. (2018)).
1.2.2. The uniqueness of the Iberian Peninsula
The Iberian Peninsula, like Italy and the Balkans, was a refuge during the Ice Age, preserving a unique diversity. The earliest evidence of dogs dates from 7,900 to 7,600 years ago in archaeological contexts accumulated by hunter-gatherer societies, a few centuries before the arrival of the first Neolithic communities.
By analyzing the remains of five Mesolithic dogs and 15 samples of dogs dating from the Roman period, collected from archaeological sites in Portugal, the authors show a high frequency of mitochondrial haplogroup A, the majority in present-day dogs. Eighty percent of the Mesolithic sequences from Portugal belong to this haplogroup. This result provides evidence that haplogroup A was present in Europe before the Neolithic period. Until now, haplogroup C was considered the most common clade in Europe before the Neolithic era (Frantz et al. 2016). Haplogroup A, observed at higher frequencies in the Middle East and Asia, had been considered to have been introduced to Europe after the arrival of Neolithic farmers, perhaps in the Bronze Age (Ollivier et al. 2018). These results suggest, in contrast, that this haplogroup may have been present in European refuges prior to Neolithic influence. These Mesolithic dogs could be attributed to local domestication(s), which is a scenario corroborated by mitochondrial data from Paleolithic Iberian wolves. Among the samples dating from the Roman period, 12 from Portugal, Spain and Morocco belong to clade A, and three from Spain belong to clade D. So far, this is the oldest evidence of clade D in the Iberian Peninsula. This result supports the idea that there may have been significant consolidation of dog breeds from divergent genetic lineages during this period. According to these data, local breeding involving dogs of clade A and clade D in the Iberian Peninsula was continuous for at least 1,600 years. In addition, the sharing of lineages between Spanish and North African dogs may suggest genetic flow. Dogs could have been easily transported between these regions by humans following shipping trade routes.
1.2.3. Origins of the dog in America
The oldest dog records in North America are found in Alaska and Illinois, dating back 9,020 ± 85, 8,820 ± 30 and 8,840 ± 80 years, respectively (Perri et al. 2019; da Silva Coelho et al. 2021). The origins and fate of dog populations in the Americas, prior to contact with European and African peoples, have been the subject of recent study involving comparisons of ancient and modern dog genomes. Comparative genomic analyses demonstrated that the first American dogs had no ancestry with American wolves. On the contrary, these Pre-Contact Dogs (PCDs) represent a specific lineage that may have migrated from Northeast Asia across the Beringian steppe alongside humans, over 10,000 years ago. These analyses also showed that PCD populations were subsequently almost completely replaced by European dogs during the large-scale colonization of North and South America over the last 500 years. The introduction of infectious diseases during this recent colonization probably played a major role in the replacement of PCDs by European dogs.
Figure 1.4.Multiple dog introductions in North America (BP: before present)
(source: M. Ollivier, adapted from Leathoblair et al. (2019)).
The introduction of dogs into South America remains to be clarified, but most probably follows the introduction of dogs into North America via Beringia, after the arrival of humans in South America. Indeed, the oldest dog remains found in America are in the north of the continent and post-date the arrival of humans in the far south of the continent 11,000 years ago. Analysis of the mitochondrial genomes of North American dogs has shown that pre-Columbian dogs belong to a monophyletic group (haplogroup A), having diverged 14,600 years ago, sharing a common ancestor with East Siberian dogs at least 16,700 years ago. The most likely hypothesis is that they migrated with human populations from North to South America. Mitochondrial DNA analysis of several pre-Columbian Mexican dog specimens (Manin et al. 2018) supports this hypothesis. Four haplotypes belonging to haplogroup A were identified. Three of these haplotypes are common to dogs of European and American origin. These dogs, probably originating from Eurasian populations that colonized North America, reached Central and South America, where they remained isolated for several thousand years. The last haplotype, however, is close to a sequence that is only shared by modern-day Chihuahua dogs, which is thought to have originated in Mexico. This proximity suggests that it is a characteristic haplotype of pre-Columbian dogs, resulting from the genetic divergence of these local populations over the thousands of years following their introduction. Lastly, a recent phylogenetic analysis of ancient mitochondrial genomes from South American dogs confirms that pre-Columbian and modern South American dogs share a common ancestry and belong to haplogroup A. In this study, the authors also show that present-day American dogs and pre-Columbian dogs show a high degree of genetic divergence, supporting the hypothesis that pre-Columbian dogs were almost completely replaced by European dog populations after the arrival of Christopher Columbus.
1.3. From commensalism to modern breeds: identifying the genomic foundations behind the intensification of the human–dog relationship
Domestication involves an evolutionary process that documents two aspects of evolution: speciation and adaptation. In the domestication process, these two biological mechanisms consist, on the one hand, of a relative break in gene flow between the original population and the domesticated one, and, on the other hand, of a modification in selective pressures. Some studies have highlighted the importance of progressive intensification of the relationship between man and animals, leading, in the case of the dog, to a continuum from commensalism, to captive animal control, to breeding and, ultimately, to pets (Vigne 2011; Zeder 2012). Isolating, taming, controlling and moving animals into an anthropogenic ecosystem has morphological, physiological and behavioral consequences that can be identified as a sequence of common traits selected along this trajectory from wild to domesticated (Belyaev 1969; Arbuckle 2005, pp. 18–33; Trut et al. 2009). During the process of domestication, a relaxation of natural selective pressures allowed the persistence of mutations linked to these new traits, resulting in an ever-increasing divergence between the genomes of domesticated animals and those of their wild ancestors. Unlike other domesticated animals, domesticated canids have also been subject to progressive human impact on their environment, as a result of changes in socioeconomic systems and human subsistence patterns. Such shifts in cultural contexts, as well as the resulting new selective pressures, could also have had an impact on the evolution of the dog genome, by leveraging changes already in place, or enabling the emergence of new changes. In general, however, it is difficult to identify regions of the genome that are unambiguously associated with early stages of domestication, and then implicated in current phenotypic diversity. This is because (i) there may only be a very limited number of regions involved in this process, a phenomenon particularly highlighted in dogs; (ii) some traits (such as behavior) have a complex genetic basis such as multiple gene inheritance and epistatic relationships1, or are linked to regulation of gene expression; (iii) the regions identified may be large, without it being possible to accurately identify the genes or variants involved; (iv) studies are costly and time consuming (Larson and Burger 2013; Larson et al. 2014). Despite this, the change in scale of analysis (from the candidate gene to the genome) in recent years has made it possible to study the domestication process at high resolution in order to determine how it has shaped modern domesticated animals. However, understanding the basis and genetic architecture of the domestication process remains a challenge.
1.3.1. Selection and domestication markers
The mitochondrial and nuclear genomes of the dog possess an overabundance of non-synonymous mutations when compared to wolves and coyotes, which can be explained by a relaxation of selective pressures after domestication. Models suggest that once animals are freed from the selective pressures associated with life in the wild, they accumulate non-synonymous mutations under a relaxed selection regime, some of which led to new phenotypes that humans might have preferentially selected (consciously or unconsciously), while nature would have actively eliminated them. This increase in the number of non-synonymous mutations is observed in all modern dog breeds, suggesting the presence of small populations during and after domestication.
The detection of genomic loci with selective sweep signatures allows us to identify candidate regions that may have undergone rapid micro-evolution during, and shortly after, domestication. Many of the regions identified concern lipid or starch metabolism, immunity, behavior, brain function and pigmentation. These findings are consistent with the shared history of humans and domestic dogs. For example, with the development of agriculture, metabolic mechanisms to digest increasing proportions of starch from cereal crops were selected. Thus, among the candidate genes for the domestication process, the MGAM gene has been identified as being under positive selection. This gene is involved in the final stages of starch digestion. Similarly, one of the strongest selection signals between dogs and wolves is centered around CCRN4L, a gene that controls lipid metabolism through its interaction with PPAR-ϒ. The selection of this candidate gene is consistent with the change in lipid content in the diet of the earliest domestic dogs. When dogs and humans began to hunt together, the number of prey caught probably increased relative to the number caught by wolves alone, and with it, the amount of lipid consumed by early dogs. A unique dietary selective pressure may thus have resulted from both the amount of lipids consumed and the composition of the tissues made available to these dogs after humans had removed the best parts of the carcass. The dogs’ behavior was also markedly altered from that of the wolves in terms of docility and canine understanding of human facial expressions and actions. Thus, all comparisons of dog and wolf genomes revealed evidence of selection on candidate neurobehavioral genes. For example, MBP, a schizophrenia-related gene responsible for myelin sheath formation, and SH3GL2, a gene involved in synaptic vesicle formation, were found in regions identified as being under positive selection in dogs (Axelsson et al. 2013).
1.3.2. Genetic variation and adaptation to a starch-rich diet
In western Eurasia, the Neolithic transition took place between 11,500 and 6,000 years ago, with the transition from hunting and gathering to agriculture. By this time, the dog, which was domesticated during the Upper Paleolithic, had already been accompanying humans for several millennia. The study of the impact of changes in diet, which was brought about by these human societies, on the physiological changes of the first domesticated canids and the transformations in their genomes that gave rise to today’s canine genotypes and phenotypes, is of crucial importance.
A comparison of current dog and wolf genomes has identified genomic regions potentially affected by this process. In particular, a series of duplications of the gene coding for pancreatic amylase (Amy2B) appears to have been selected, leading to an increase in the number of copies of this gene in modern dogs. An increased number of Amy2B copies is associated with higher amylase activity, enabling improved starch digestion capacity (Axelsson et al. 2013). While the number of Amy2B copies widely varies in dogs (4–34 copies), the number is much lower (two to eight copies) in wolves, with 60% of wolves carrying only two copies of the gene. This suggests that dogs are better adapted to a starch-rich diet than wolves. Present-day canids show three patterns of variation in the number of Amy2B copies: (i) 60% of wolves and most dingoes carry two copies of the gene; (ii) dogs and wolves carrying between two and eight copies of Amy2B; (iii) dogs carrying more than eight copies of Amy2B. However, the question of a link between the increase in the number of Amy2B copies in dogs and the Neolithic transition remains unanswered with these data, because while this increase could have provided a strong adaptive advantage in an agricultural context, we cannot rule out that it occurred much later, following the more recent selection of specialized lineages.
Paleogenetics offers a unique opportunity to shed light on this question, through studying the genetic landscape of the varying number of Amy2B copies in ancient canid populations. The study of the number of copies of the Amy2B gene in 88 ancient dogs from various archaeological sites across Eurasia yielded results for 13 of them. Four of the ancient dogs – from Romania (6,500 years ago), Turkmenistan and France (4,000–5,000 years ago) – possessed more than eight copies of Amy2B. The hypothesis of a modern origin explaining the increase in the number of copies is ruled out. The earliest expansion of the Amy2B gene number could be dated to 7,000 years ago (Neolithic era) and probably constituted an important adaptive advantage for dogs that were able to feed on the waste or remains of human meals (Ollivier et al. 2016). Interestingly, five of the samples appear to only possess two copies, which is a situation that is almost nonexistent in present-day dogs. Dog populations with low Amy2B copy numbers are currently associated with nonagricultural populations (Arent 2016). This pattern supports the hypothesis of an ancient expansion of Amy2B associated with the Neolithic period. Ultimately, it is worth noting that individuals presenting the three profiles (two copies, three to eight copies, more than eight copies) can be found on the same archaeological sites, which shows that in the Neolithic era, the expansion of the Amy2B gene was not yet fixed in dog populations associated with Neolithic agricultural societies. These results have recently been corroborated (Bergstrom et al. 2020) by showing that several Neolithic dogs (Iran: 5,800 years old; Spain: 6,200 years old) do indeed possess a high number of copies of the Amy2B gene. This increase, which was variable among dog populations associated with the first farmers, was widespread and fixed for a few thousand years with the regular use of starch-rich agricultural products.
