Animal evolution during domestication: the domesticated fox as a model

We review the evolution of domestic animals, emphasizing the effect of the earliest steps of domestication on its course. Using the first domesticated species, the dog (Canis familiaris), for illustration, we describe the evolutionary peculiarities during the historical domestication, such as the high level and wide range of diversity. We suggest that the process of earliest domestication via unconscious and later conscious selection of human‐defined behavioral traits may accelerate phenotypic variations. The review is based on the results of a long‐term experiment designed to reproduce early mammalian domestication in the silver fox (Vulpes vulpes) selected for tameability or amenability to domestication. We describe changes in behavior, morphology and physiology that appeared in the fox during its selection for tameability, which were similar to those observed in the domestic dog. Based on the data of the fox experiment and survey of relevant data, we discuss the developmental, genetic and possible molecular genetic mechanisms underlying these changes. We ascribe the causative role in evolutionary transformation of domestic animals to the selection for behavior and to the neurospecific regulatory genes it affects.     

Evaluating the self‐domestication hypothesis of human evolution

“Self‐domestication” has been invoked to understand important aspects of human evolution, integrating physiological, behavioral, and morphological information in a novel way. It proposes that selection for reduced aggression on animals undergoing domestication provides a model for selection favoring prosocial behaviors in humans and for a set of seemingly independent features, which arose as a result of developmental correlation. We review the history of the idea and examine patterns of domestication. A lack of empirical studies on evolutionary rates and variation thwarts meaningful comparison with domestication. The neural crest hypothesis for domestication has great explanatory power but it is difficult to test. We suggest a scenario in which the morphological byproducts of domestication can act as an honest signal of reduced xenophobia. Future studies should test if alternative explanations for the features deemed to result from self‐domestication are mutually exclusive and generate data to test predictions of these hypotheses.     

群体遗传学下动物驯化研究进展

动物驯化是将野生动物改变为能够长期稳定饲养的家养动物的过程。作为新石器时代农业革命的内容,驯化是人类社会文明进步的重要标志之一。由于和人类的密切关系,驯化不仅改变了动物的野生状态,也改变了人类的生活习性和文明进程。动物驯化研究的关键问题包含驯化祖先是谁、驯化所产生的改变及驯化时间地点等。随着高通量基因组技术和对应分析方法的发展,目前研究动物驯化一般基于群体水平,在群体遗传学的框架下研究动物驯化过程中的重要事件。本文总结了群体遗传学下动物驯化研究的相关内容,包括群体动态历史、选择信号、基因交流等,着重介绍了基因选择初始时间和基因交流时间两个新的拓展内容及分析方法,概述了家猪(Sus scrofa f.domestica)、家鸡(Gallus gallus domesticus)、绵羊(Ovis aries)和山羊(Caprine hircus)等几种主要农业动物近期驯化研究的进展,以期为动物驯化研究提供了新的方向和视角。     

Domestication of cereal crops in the old world: in search of a new approach to solving old problem

N.I. Vavilov's theory of the centres of origin of cultivated plants is still as a methodological base for studying processes of domestication. This theory, along with archaeological, botanical, and molecular genetic data, helped to determine the most probable regions where the principal cultivated species were introduced into culture. The search for the mechanisms of origins of morphological changes in the course of domestication is one of evolutionary biology's oldest problems. Employing novd molecular biological data for solving this problem provides a key to the understanding of these mechanisms and helps to reconstruct a possible scenario of how the traits that distinguish domesticated plants from their wild relatives got involved into selection. It is hypothesized that distinct physiological and morphological differences important to ancient agrarians originated from quantitative and/or qualitative changes in the loci regulating the programmes of plant ontogeny. This hypothesis helps to reveal the mechanisms of origin of certain traits in the course of domestication, to study the connection between the direction of selection and how such traits are genetically controlled, and to outline particular ways for further detailed studies of the evolutionary aspect of domestication processes.     

Evolutionary pets: offspring numbers reveal speciation process in domesticated chickens

Since Darwin, the nature of the relationship between evolution and domestication has been debated. Evolution offers different mechanisms of selection that lead to adaptation and may end in the origin of new species as defined by the biological species concept. Domestication has given rise to numerous breeds in almost every domesticated species, including chickens. At the same time, so-called artificial selection seems to exclude mechanisms of sexual selection by the animals themselves. We want to forward the question to the animal itself: With whom do you reproduce successfully? This study focused on the sexual behavior of the domestic chicken Gallus gallus f.dom., particularly the White Crested Polish breed. Experiments on mate choice and the observation of fertilization and hatching rates of mixed-breeding groups revealed breed-specific preferences. In breeding groups containing White Crested Polish and a comparative breed, more purebred chicks hatched than hybrids (number of eggs collected: 1059). Mating was possible in equal shares, but in relation to the number of eggs collected, purebred offspring (62.75%±7.10%, M±SE) hatched to a greater extend compared to hybrid offspring (28.75%±15.32%, M±SE). These data demonstrate that the mechanism of sexual selection is still present in domestic chicken breeds, which includes the alteration of gene frequencies typical for domestication and evolutionary speciation. Due to selection and mate choice we state that breeding in principle can generate new species. Therefore, we see domestication as an evolutionary process that integrates human interests of animal breeding with innate mate choice by the animal.     

An Experiment on Fox Domestication and Debatable Issues of Evolution of the Dog

This paper is a review of the results of the authors obtained in a long-term experiment on fox domestication. Debatable issues of dog evolution are discussed in light of these results. It is demonstrated that genetic physiological mechanisms of the behavior transformation during selection and the nature of the arising phenotypic changes are associated with retarded development of corresponding ontogenetic processes. As a result of this retardation, the adult animals retain juvenile traits of behavior and morphology (the phenomenon of neoteny). The role of hormonal changes caused by domestication in the evolutionary origin of neoteny is discussed.     

Evolutionary domestication in Drosophila subobscura

The domestication of plants and animals is historically one of the most important topics in evolutionary biology. The evolutionary genetic changes arising from human cultivation are complex because of the effects of such varied processes as continuing natural selection, artificial selection, deliberate inbreeding, genetic drift and hybridization of different lineages. Despite the interest of domestication as an evolutionary process, few studies of multicellular sexual species have approached this topic using well-replicated experiments. Here we present a comprehensive study in which replicated evolutionary trajectories from several Drosophila subobscura populations provide a detailed view of the evolutionary dynamics of domestication in an outbreeding animal species. Our results show a clear evolutionary response in fecundity traits, but no clear pattern for adult starvation resistance and juvenile traits such as development time and viability. These results supply new perspectives on the confounding of adaptation with other evolutionary mechanisms in the process of domestication.     

An experiment on fox domestication and debatable issues of evolution of the dog

This paper is a review of the results of the authors obtained in a long-term experiment on fox domestication. Debatable issues of dog evolution are discussed in light of these results. It is demonstrated that genetic physiological mechanisms of the behavior transformation during selection and the nature of the arising phenotypic changes are associated with retarded development of corresponding ontogenetic processes. As a result of this retardation, the adult animals retain juvenile traits of behavior and morphology (the phenomenon of neoteny). The role of hormonal changes caused by domestication in the evolutionary origin of neoteny is discussed.     

Morphofunctional status of the adrenal cortex in female silver foxes and the effect of domestication and photoperiodic conditions

Studies on 7-day-old and 8-month-old female silver foxes indicate that additional photostimulation affects to a various extent morphological and functional condition of the adrenal cortex in animals selected and unselected for the domestication type of behaviour. In relatively wild foxes, additional illumination stimulated the activity of the reticular zone, whereas in domesticated animals the same photoperiod increased the activity in the fascicular zone. It is suggested that selection of silver foxes for the domestication type of behaviour affects the sensitivity of the adrenals to external illumination.     

Structural Variants Selected during Yak Domestication Inferred from Long-Read Whole-Genome Sequencing

Structural variants (SVs) represent an important genetic resource for both natural and artificial selection. Here we present a chromosome-scale reference genome for domestic yak (Bos grunniens) that has longer contigs and scaffolds (N50 44.72 and 114.39 Mb, respectively) than reported for any other ruminant genome. We further obtained long-read resequencing data for 6 wild and 23 domestic yaks and constructed a genetic SV map of 372,220 SVs that covers the geographic range of the yaks. The majority of the SVs contains repetitive sequences and several are in or near genes. By comparing SVs in domestic and wild yaks, we identified genes that are predominantly related to the nervous system, behavior, immunity, and reproduction and may have been targeted by artificial selection during yak domestication. These findings provide new insights in the domestication of animals living at high altitude and highlight the importance of SVs in animal domestication.     

ARCHAEOLOGICAL DATA REVEAL SLOW RATES OF EVOLUTION DURING PLANT DOMESTICATION

Domestication is an evolutionary process of species divergence in which morphological and physiological changes result from the cultivation/tending of plant or animal species by a mutualistic partner, most prominently humans. Darwin used domestication as an analogy to evolution by natural selection although there is strong debate on whether this process of species evolution by human association is an appropriate model for evolutionary study. There is a presumption that selection under domestication is strong and most models assume rapid evolution of cultivated species. Using archaeological data for 11 species from 60 archaeological sites, we measure rates of evolution in two plant domestication traits—nonshattering and grain/seed size increase. Contrary to previous assumptions, we find the rates of phenotypic evolution during domestication are slow, and significantly lower or comparable to those observed among wild species subjected to natural selection. Our study indicates that the magnitudes of the rates of evolution during the domestication process, including the strength of selection, may be similar to those measured for wild species. This suggests that domestication may be driven by unconscious selection pressures similar to that observed for natural selection, and the study of the domestication process may indeed prove to be a valid model for the study of evolutionary change.     

Detection of signatures of selective sweeps in the Blonde d'Aquitaine cattle breed

Identifying recent positive selection signatures in domesticated animals could provide information on genome response to strong directional selection from domestication and artificial selection and therefore could help in identifying mutations responsible for improved traits. We used genotyping data generated using Illumina's BovineSNP50 Genotyping BeadChips to identify selection signatures in the Blonde d'Aquitaine breed, a well‐muscled French beef breed. For this purpose, we employed a hidden Markov model‐based test, which detects selection by studying local variations in the allele frequency spectrum along the genome, within a single population. Three regions containing selective sweeps were identified. Annotation of genes located within these regions revealed interesting candidate genes. For example, myostatin (also known as GDF8), a known muscle growth factor inhibitor, is located within the selection signature region found on chromosome 2. In addition, we have identified chromosomal regions that show some evidence of selection within QTL regions for economically important traits. The results of this study could help to better understand the mechanisms related to the selection of the Blonde d'Aquitaine breed.     

Evolutionary history of pearl millet (Pennisetum glaucum [L.] R. Br.) and selection on flowering genes since its domestication

The plant domestication process is associated with considerable modifications of plant phenotype. The identification of the genetic basis of this adaptation is of great interest for evolutionary biology. One of the methods used to identify such genes is the detection of signatures of selection. However, domestication is generally associated with major demographic effects. It is therefore crucial to disentangle the effects of demography and selection on diversity. In this study, we investigated selection in a flowering time pathway during domestication of pearl millet. We first used a random set of 20 genes to model pearl millet domestication using approximate Bayesian computation. This analysis showed that a model with exponential growth and wild-cultivated gene flow was well supported by our data set. Under this model, the domestication date of pearl millet is estimated at around 4,800 years ago. We assessed selection in 15 pearl millet DNA sequences homologous to flowering time genes and showed that these genes underwent selection more frequently than expected. We highlighted significant signatures of selection in six pearl millet flowering time genes associated with domestication or improvement of pearl millet. Moreover, higher deviations from neutrality were found for circadian clock-associated genes. Our study provides new insights into the domestication process of pearl millet and shows that a category of genes of the flowering pathway were preferentially selected during pearl millet domestication.     

Methodological approach to genetic-selection analysis of social behavior of animals (Using as an example domestic behavior of the silver fox

Social behaviour of animals, i.e. interspecies contacts, were studied in a population of silver foxes in the longitudinal model domestication experiment. Three social behaviour traits were analysed: contactibility, critical distance and domestication index. The latter trait is a linear function of elementary behaviour reactions, postures induced by man which is determined by the principal components method. The most valiable selection phenotype for further modelling of domestication, as shown by the capacity to adequately reflect a pattern of genotype--environment interaction, the structure of correlation ratios for different forms of behaviour and the level of genetic relationships between relatives, is the domestication index.     

Largely unlinked gene sets targeted by selection for domestication syndrome phenotypes in maize and sorghum

The domestication of diverse grain crops from wild grasses was a result of artificial selection for a suite of overlapping traits producing changes referred to in aggregate as ‘domestication syndrome’. Parallel phenotypic change can be accomplished by either selection on orthologous genes or selection on non‐orthologous genes with parallel phenotypic effects. To determine how often artificial selection for domestication traits in the grasses targeted orthologous genes, we employed resequencing data from wild and domesticated accessions of Zea (maize) and Sorghum (sorghum). Many ‘classic’ domestication genes identified through quantitative trait locus mapping in populations resulting from wild/domesticated crosses indeed show signatures of parallel selection in both maize and sorghum. However, the overall number of genes showing signatures of parallel selection in both species is not significantly different from that expected by chance. This suggests that while a small number of genes will extremely large phenotypic effects have been targeted repeatedly by artificial selection during domestication, the optimization part of domestication targeted small and largely non‐overlapping subsets of all possible genes which could produce equivalent phenotypic alterations.     

Classic Selective Sweeps Revealed by Massive Sequencing in Cattle

Human driven selection during domestication and subsequent breed formation has likely left detectable signatures within the genome of modern cattle. The elucidation of these signatures of selection is of interest from the perspective of evolutionary biology, and for identifying domestication-related genes that ultimately may help to further genetically improve this economically important animal. To this end, we employed a panel of more than 15 million autosomal SNPs identified from re-sequencing of 43 Fleckvieh animals. We mainly applied two somewhat complementary statistics, the integrated Haplotype Homozygosity Score (iHS) reflecting primarily ongoing selection, and the Composite of Likelihood Ratio (CLR) having the most power to detect completed selection after fixation of the advantageous allele. We find 106 candidate selection regions, many of which are harboring genes related to phenotypes relevant in domestication, such as coat coloring pattern, neurobehavioral functioning and sensory perception including KIT, MITF, MC1R, NRG4, Erbb4, TMEM132D and TAS2R16, among others. To further investigate the relationship between genes with signatures of selection and genes identified in QTL mapping studies, we use a sample of 3062 animals to perform four genome-wide association analyses using appearance traits, body size and somatic cell count. We show that regions associated with coat coloring significantly (P<0.0001) overlap with the candidate selection regions, suggesting that the selection signals we identify are associated with traits known to be affected by selection during domestication. Results also provide further evidence regarding the complexity of the genetics underlying coat coloring in cattle. This study illustrates the potential of population genetic approaches for identifying genomic regions affecting domestication-related phenotypes and further helps to identify specific regions targeted by selection during speciation, domestication and breed formation of cattle. We also show that Linkage Disequilibrium (LD) decays in cattle at a much faster rate than previously thought.     

Genome-wide analysis of the world's sheep breeds reveals high levels of historic mixture and strong recent selection

Through their domestication and subsequent selection, sheep have been adapted to thrive in a diverse range of environments. To characterise the genetic consequence of both domestication and selection, we genotyped 49,034 SNP in 2,819 animals from a diverse collection of 74 sheep breeds. We find the majority of sheep populations contain high SNP diversity and have retained an effective population size much higher than most cattle or dog breeds, suggesting domestication occurred from a broad genetic base. Extensive haplotype sharing and generally low divergence time between breeds reveal frequent genetic exchange has occurred during the development of modern breeds. A scan of the genome for selection signals revealed 31 regions containing genes for coat pigmentation, skeletal morphology, body size, growth, and reproduction. We demonstrate the strongest selection signal has occurred in response to breeding for the absence of horns. The high density map of genetic variability provides an in-depth view of the genetic history for this important livestock species.     

Domestication Process of the Goat Revealed by an Analysis of the Nearly Complete Mitochondrial Protein-Encoding Genes

Goats (Capra hircus) are one of the oldest domesticated species, and they are kept all over the world as an essential resource for meat, milk, and fiber. Although recent archeological and molecular biological studies suggested that they originated in West Asia, their domestication processes such as the timing of population expansion and the dynamics of their selection pressures are little known. With the aim of addressing these issues, the nearly complete mitochondrial protein-encoding genes were determined from East, Southeast, and South Asian populations. Our coalescent time estimations suggest that the timing of their major population expansions was in the Late Pleistocene and significantly predates the beginning of their domestication in the Neolithic era (≈10,000 years ago). The ω (ratio of non-synonymous rate/synonymous substitution rate) for each lineage was also estimated. We found that the ω of the globally distributed haplogroup A which is inherited by more than 90% of goats examined, turned out to be extremely low, suggesting that they are under severe selection pressure probably due to their large population size. Conversely, the ω of the Asian-specific haplogroup B inherited by about 5% of goats was relatively high. Although recent molecular studies suggest that domestication of animals may tend to relax selective constraints, the opposite pattern observed in our goat mitochondrial genome data indicates the process of domestication is more complex than may be presently appreciated and cannot be explained only by a simple relaxation model.     

Artificial Selection and Domestication: Modern Lessons from Darwin’s Enduring Analogy

It is clear from his published works that Charles Darwin considered domestication to be very useful in exploring and explaining mechanisms of evolutionary change. Not only did domestication occupy the introductory chapter of On the Origin of Species, but he revisited the topic in a two-volume treatise less than a decade later. In addition to drawing much of his information about heredity from studies of domesticated animals and plants, Darwin saw important parallels between the process of artificial selection by humans and natural selection by the environment. There was resistance to this analogy even among Darwin’s contemporary supporters when it was proposed, and there also has been disagreement among historians and philosophers regarding the role that the analogy with artificial selection actually played in the discovery of natural selection. Regardless of these issues, the analogy between artificial and natural selection remains important in both research and education in evolution. In particular, the present article reviews ten lessons about evolution that can be drawn from the modern understanding of domestication and artificial selection. In the process, a basic overview is provided of current approaches and knowledge in this rapidly advancing field.

White-tailed Deer Management Strategies and Domestication Processes

Today, people in the U.S. commonly engage in mutual relationships with white-tailed deer (WTD) in manners consistent with those that ultimately resulted in the domestication of animals in the past. Using a wide range of media depicting perspectives of sport hunters, biologists, ecologists, and game managers this paper explores: 1) the influence of anthropogenic environments on WTD behavior, 2) ‘game’ management and the ability to create valued demographics, and 3) the selection for increased antler size in farmed WTD. This study demonstrates that in order to gain a more accurate understanding of domestication, analyses should focus on the evolution of mutualisms between people and animals. Insights gleamed from this analysis also contribute toward our archaeological understanding of prehistoric animal domestication.