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.     

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.     

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.     

Kind granddaughters of angry grandmothers: The effect of domestication on vocalization in cross-bred silver foxes

The genetic basis of the effects of domestication has previously been examined in relation to morphological, physiological and behavioural traits, but not for vocalizations. According to Belyaev [Belyaev, D.K., 1979. Destabilizing selection as a factor in domestication. J. Hered. 70, 301-308], directional selection for tame behaviour toward humans resulted in domestication. This hypothesis has been confirmed experimentally on the farm-bred silver fox Vulpes vulpes population that has undergone 45 years of artificial selection for tameness and 35 years of selection for aggressiveness. These foxes, with their precisely known attitudes toward people, provide a means of examining vocal indicators of tameness and aggressiveness to establish the genetic basis for vocal production in canids. We examined vocalizations toward people in foxes selected for tameness and aggressiveness compared to those of three kinds of crosses: Hybrids (Tame × Aggressive), A-Backcrosses (Aggressive × Hybrid) and T-Backcrosses (Tame × Hybrid). We report the effects of selection for tameness on usage and structure of different vocalizations and suggest that vocal indicators for tameness and aggressiveness toward people are discrete phenotypic traits in silver foxes.     

Social cognitive evolution in captive foxes is a correlated by-product of experimental domestication

Dogs have an unusual ability for reading human communicative gestures (e.g., pointing) in comparison to either nonhuman primates (including chimpanzees) or wolves . Although this unusual communicative ability seems to have evolved during domestication , it is unclear whether this evolution occurred as a result of direct selection for this ability, as previously hypothesized , or as a correlated by-product of selection against fear and aggression toward humans--as is the case with a number of morphological and physiological changes associated with domestication . We show here that fox kits from an experimental population selectively bred over 45 years to approach humans fearlessly and nonaggressively (i.e., experimentally domesticated) are not only as skillful as dog puppies in using human gestures but are also more skilled than fox kits from a second, control population not bred for tame behavior (critically, neither population of foxes was ever bred or tested for their ability to use human gestures) . These results suggest that sociocognitive evolution has occurred in the experimental foxes, and possibly domestic dogs, as a correlated by-product of selection on systems mediating fear and aggression, and it is likely the observed social cognitive evolution did not require direct selection for improved social cognitive ability.     

Breeding of the Russian sable: Stages of industrial domestication and genetic variability

Creating farms for sable breeding was associated with the commercial destruction of natural populations and, consequently, the overall decline in the species number. The gene pool of the first farm-bred sable population in Russia, established in the vicinity of Moscow (“Pushkinskiy” fur farm), was formed by crossing of animals removed from nine natural populations. In the first eight years of farm operation, approximately one thousand animals were used for sable breeding; some of these animals were able to adapt to the farm management and, subsequently, to the selection for a number of quantitative traits in the period of industrial domestication. It took about ten years for breeders to work out the breeding and selection technologies, which became successfully employed in the established affiliated sable breeding farms. The main achievement in sable breeding over the 85-year historical period of breeding in Russia is the creation of two unique breeds, black sable (1969) and Saltykovskaya 1 (2007). In general, industrial domestication in fur farming and the subsequent breeding works made the fur of many species (mink, fox, Arctic fox) obtained from natural populations uncompetitive, which undoubtedly reduced the hunting interest in the animals living in the wild. Consequently, hunting for fur-bearing animals of most species decreased and has only local importance. Owing to the specific features of sable biology, the fur of farm-bred animals cannot yet completely replace the furs obtained by hunting; however, the farm-bred sable population is constantly growing. This review presents the results of the analysis of the level of genetic variability in natural and farm populations at nuclear and mitochondrial loci. The comparative analysis makes it possible to estimate the loss of genetic diversity upon the species adaptation to the new conditions of existence.     

A striking example of developmental bias in an evolutionary process: The “domestication syndrome”

The question of whether “developmental bias” can influence evolution is still controversial, despite much circumstantial evidence and a good theoretical argument. Here, I will argue that the domestication of mammalian species, which took place independently more than two dozen times, provides a particularly convincing example of developmental bias in evolution. The singular finding that underlies this claim is the repeated occurrence in domesticated mammals of a set of distinctive traits, none of which were deliberately selected. This phenomenon has been termed “the domestication syndrome”. In this article, I will: (a) describe the properties of the domestication syndrome; (b) show how it can be explained in terms of the operation of a specific genetic regulatory network, that which governs neural crest cell development; and (c) discuss Dmitry Belyaev's idea of “destabilizing selection,” which holds that selecting for a new behavior often entails neuroendocrine alterations that alter many aspects of development. Finally, I will argue for the potential general significance of such destabilizing selection, in combination with developmental bias, in animal evolution.     

Genotyping-By-Sequencing (GBS) Detects Genetic Structure and Confirms Behavioral QTL in Tame and Aggressive Foxes (Vulpes vulpes)

The silver fox (Vulpes vulpes) offers a novel model for studying the genetics of social behavior and animal domestication. Selection of foxes, separately, for tame and for aggressive behavior has yielded two strains with markedly different, genetically determined, behavioral phenotypes. Tame strain foxes are eager to establish human contact while foxes from the aggressive strain are aggressive and difficult to handle. These strains have been maintained as separate outbred lines for over 40 generations but their genetic structure has not been previously investigated. We applied a genotyping-by-sequencing (GBS) approach to provide insights into the genetic composition of these fox populations. Sequence analysis of EcoT22I genomic libraries of tame and aggressive foxes identified 48,294 high quality SNPs. Population structure analysis revealed genetic divergence between the two strains and more diversity in the aggressive strain than in the tame one. Significant differences in allele frequency between the strains were identified for 68 SNPs. Three of these SNPs were located on fox chromosome 14 within an interval of a previously identified behavioral QTL, further supporting the importance of this region for behavior. The GBS SNP data confirmed that significant genetic diversity has been preserved in both fox populations despite many years of selective breeding. Analysis of SNP allele frequencies in the two populations identified several regions of genetic divergence between the tame and aggressive foxes, some of which may represent targets of selection for behavior. The GBS protocol used in this study significantly expanded genomic resources for the fox, and can be adapted for SNP discovery and genotyping in other canid species.     

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.     

Genetics of behavior in the silver fox

The silver fox provides a rich resource for investigating the genetics of behavior, with strains developed by intensely selective breeding that display markedly different behavioral phenotypes. Until recently, however, the tools for conducting molecular genetic investigations in this species were very limited. In this review, the history of development of this resource and the tools to exploit it are described. Although the focus is on the genetics of domestication in the silver fox, there is a broader context. In particular, one expectation of the silver fox research is that it will be synergistic with studies in other species, including humans, to yield a more comprehensive understanding of the molecular mechanisms and evolution of a wider range of social cognitive behaviors.     

A genome-wide scan for signatures of directional selection in domesticated pigs

Background

Animal domestication involved drastic phenotypic changes driven by strong artificial selection and also resulted in new populations of breeds, established by humans. This study aims to identify genes that show evidence of recent artificial selection during pig domestication.

Results

Whole-genome resequencing of 30 individual pigs from domesticated breeds, Landrace and Yorkshire, and 10 Asian wild boars at ~16-fold coverage was performed resulting in over 4.3 million SNPs for 19,990 genes. We constructed a comprehensive genome map of directional selection by detecting selective sweeps using an F_ST-based approach that detects directional selection in lineages leading to the domesticated breeds and using a haplotype-based test that detects ongoing selective sweeps within the breeds. We show that candidate genes under selection are significantly enriched for loci implicated in quantitative traits important to pig reproduction and production. The candidate gene with the strongest signals of directional selection belongs to group III of the metabolomics glutamate receptors, known to affect brain functions associated with eating behavior, suggesting that loci under strong selection include loci involved in behaviorial traits in domesticated pigs including tameness.

Conclusions

We show that a significant proportion of selection signatures coincide with loci that were previously inferred to affect phenotypic variation in pigs. We further identify functional enrichment related to behavior, such as signal transduction and neuronal activities, for those targets of selection during domestication in pigs.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-015-1330-x) contains supplementary material, which is available to authorized users.     

Plant domestication: a model for studying the selection of linkage

The process of domestication leads to acquisition of traits that are often similar between plant species that belong to the same family but have different breeding systems. Hence domestication is a useful model for studying evolutionary responses to selection in plants with contrasting breeding systems. We consider a stochastic model simulating gene flow between a natural population and an initial population containing mutants with domesticated phenotypes at low frequency. We assume that a large number of loci contribute equally to the cultivated phenotype. Our results indicate that the number of loci for which the mutant (‘domestication’) allele is maintained is larger in autogamous plants than in allogamous ones and that domestication can lead to the selection of tightly linked combinations of genes in allogamous plants. This work provides a general model for the selection of gene clusters through a sieve effect and it is discussed in comparison with models proposed to explain the evolution of linkage of genes determining wing patterns in butterflies exhibiting Batesian mimicry.     

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.     

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.     

Sex ratio in silver foxes: effects of domestication and the star gene

The course of changes in secondary sex ratio (proportion of males at birth) in silver foxes bred at the fur farm of this Institute was analyzed. Data collected over several years of breeding of a domesticated (experimental) population selected for amenability to domestication and of a commercial (control) were compared. A tendency to increase in secondary sex ratio was demonstrated in both populations. However, the proportion of males at birth was higher in domestic foxes. This proportion, calculated from the combined data for 1978–1993, was 0.538±0.005 and 0.511±0.007 in the selected and commercial populations, respectively. The minimal departure of the observed sex ratio from 0.5 was demonstrated for litters with five pups, which is close to the average litter size in fox populations. The proportion of males increases with both increasing and decreasing litter size. An analysis of secondary sex ratio with respect to maternal age revealed a minimal departure of sex ratio from the expected in offspring from foxes of optimal reproductive age (2–4 years). An effect of the autosomal semidominant coat color mutation star on male excess at birth was also found: secondary sex ratio was higher (0.583±0.015) in offspring of mothers heterozygous for the star mutation than from standard types of the domesticated population. The increase in secondary sex ratio in the analyzed fox populations is viewed as a correlated response to selection for domestication. The hormonal mechanisms mediating the effects of both this selection and the star mutation on sex ratio at birth are discussed.     

An Integrated Hypothesis on the Domestication of Bactris gasipaes

Peach palm (Bactris gasipaes Kunth) has had a central place in the livelihoods of people in the Americas since pre-Columbian times, notably for its edible fruits and multi-purpose wood. The botanical taxon includes both domesticated and wild varieties. Domesticated var gasipaes is believed to derive from one or more of the three wild types of var. chichagui identified today, although the exact dynamics and location of the domestication are still uncertain. Drawing on a combination of molecular and phenotypic diversity data, modeling of past climate suitability and existing literature, we present an integrated hypothesis about peach palm’s domestication. We support a single initial domestication event in south western Amazonia, giving rise to var. chichagui type 3, the putative incipient domesticate. We argue that subsequent dispersal by humans across western Amazonia, and possibly into Central America allowed for secondary domestication events through hybridization with resident wild populations, and differential human selection pressures, resulting in the diversity of present-day landraces. The high phenotypic diversity in the Ecuadorian and northern Peruvian Amazon suggest that human selection of different traits was particularly intense there. While acknowledging the need for further data collection, we believe that our results contribute new insights and tools to understand domestication and dispersal patterns of this important native staple, as well as to plan for its conservation.     

A marker set for construction of a genetic map of the silver fox (Vulpes vulpes)

The silver fox, a variant of the red fox (Vulpes vulpes), is a close relative of the dog (Canis familiaris). Cytogenetic differences and similarities between these species are well understood, but their genomic organizations have not been compared at higher resolution. Differences in their behavior also remain unexplained. Two silver fox strains demonstrating markedly different behavior have been generated at the Institute of Cytology and Genetics of the Russian Academy of Sciences. Foxes selected for tameness are friendly, like domestic dogs, while foxes selected for aggression resist human contact. To refine our understanding of the comparative genomic organization of dogs and foxes, and enable a study of the genetic basis of behavior in these fox strains, we need a meiotic linkage map of the fox. Towards this goal we generated a primary set of fox microsatellite markers. Four hundred canine microsatellites, evenly distributed throughout the canine genome, have been identified that amplify robustly from fox DNA. Polymorphism information content (PIC) values were calculated for a representative subset of these markers and population inbreeding coefficients were determined for tame and aggressive foxes. To begin to identify fox-specific single nucleotide polymorphisms (SNPs) in genes involved in the neurobiology of behavior, fox and dog orthologs of serotonin 5-HT1A and 5-HT1B receptor genes have been cloned. Sequence comparison of these genes from tame and aggressive foxes reveal several SNPs. The close relationship of the fox and dog enables canine genomic tools to be utilized in developing a fox meiotic map and mapping behavioral traits in the fox.     

The domestication of American wildrice

The expansion in wildrice (Zizania palustris) production and the associated research efforts represent the largest modern effort to domesticate a cereal grain. Wildrice growers brought the species under cultivation, but plant breeding and agronomic research have accelerated the domestication process. The domestication and commercialization of this diploid (2n = 30), protogynous, cross-pollinated, annual, aquatic cereal present an opportunity to examine crop evolution and domestication theory. Traits associated with the domesticated cereal grains are shattering resistance, tiller synchrony, and increased seed size. This syndrome of traits may result from automatic selection, the selective force applied by repeated cycles of planting of harvested seed. Positive responses from deliberate selection for these traits in wildrice populations indicate that a domestication ideotype is attainable through plant breeding and that founder effect in this diploid species may be negligible. Continued commercial production of wildrice in the Great Lakes region is not likely to further the domestication process, whereas automatic selection may be initiated in the emerging California wildrice industry.     

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.     

家养动物驯化起源的研究方法与进展

驯化动物伴随了人类上万年的进化历程。在驯化过程中, 家养动物表型和行为特征发生巨大改变, 并与人类生产生活的进步相适应。研究动物驯化问题对于了解遗传多样性及适应性进化, 解析复杂性状的遗传机制等具有重要的意义, 成为生物学领域的重点研究内容之一。本文专注于动物驯化的初始阶段, 首先介绍了驯化起源的时间与地点、驯化途径和驱动因、驯化后的扩散和品种选育; 其次从驯化对象的角度着重介绍了考古学、分子和群体遗传学两方面的家养动物驯化起源的研究策略、优势与不足, 以及未来的发展方向; 最后, 我们综合多方面的证据, 介绍了在中国驯化的家猪(Sus domesticus)和家鸡(Gallus gallus domesticus)以及其他主要家养动物考古和分子水平上驯化起源的研究进展。本文整合多种证据为家养动物驯化起源的研究提供了相对完整的视角和新的思路。