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.     

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.     

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.     

Comparative population genomics identified genomic regions and candidate genes associated with fruit domestication traits in peach

Crop evolution is a long‐term process involving selection by natural evolutionary forces and anthropogenic influences; however, the genetic mechanisms underlying the domestication and improvement of fruit crops have not been well studied to date. Here, we performed a population structure analysis in peach (Prunus persica) based on the genome‐wide resequencing of 418 accessions and confirmed the presence of an obvious domestication event during evolution. We identified 132 and 106 selective sweeps associated with domestication and improvement, respectively. Analysis of their tissue‐specific expression patterns indicated that the up‐regulation of selection genes during domestication occurred mostly in fruit and seeds as opposed to other organs. However, during the improvement stage, more up‐regulated selection genes were identified in leaves and seeds than in the other organs. Genome‐wide association studies (GWAS) using 4.24 million single nucleotide polymorphisms (SNPs) revealed 171 loci associated with 26 fruit domestication traits. Among these loci, three candidate genes were highly associated with fruit weight and the sorbitol and catechin content in fruit. We demonstrated that as the allele frequency of the SNPs associated with high polyphenol composition decreased during peach evolution, alleles associated with high sugar content increased significantly. This indicates that there is genetic potential for the breeding of more nutritious fruit with enhanced bioactive polyphenols without disturbing a harmonious sugar and acid balance by crossing with wild species. This study also describes the development of the genomic resources necessary for evolutionary research in peach and provides the large‐scale characterization of key agronomic traits in this crop species.     

Plant domestication slows pest evolution

Agricultural practices such as breeding resistant varieties and pesticide use can cause rapid evolution of pest species, but it remains unknown how plant domestication itself impacts pest contemporary evolution. Using experimental evolution on a comparative phylogenetic scale, we compared the evolutionary dynamics of a globally important economic pest – the green peach aphid (Myzus persicae) – growing on 34 plant taxa, represented by 17 crop species and their wild relatives. Domestication slowed aphid evolution by 13.5%, maintained 10.4% greater aphid genotypic diversity and 5.6% higher genotypic richness. The direction of evolution (i.e. which genotypes increased in frequency) differed among independent domestication events but was correlated with specific plant traits. Individual‐based simulation models suggested that domestication affects aphid evolution directly by reducing the strength of selection and indirectly by increasing aphid density and thus weakening genetic drift. Our results suggest that phenotypic changes during domestication can alter pest evolutionary dynamics.     

A draft genome of sweet cherry (Prunus avium L.) reveals genome‐wide and local effects of domestication

Sweet cherry (Prunus avium L.) trees are both economically important fruit crops but also important components of natural forest ecosystems in Europe, Asia and Africa. Wild and domesticated trees currently coexist in the same geographic areas with important questions arising on their historical relationships. Little is known about the effects of the domestication process on the evolution of the sweet cherry genome. We assembled and annotated the genome of the cultivated variety “Big Star*” and assessed the genetic diversity among 97 sweet cherry accessions representing three different stages in the domestication and breeding process (wild trees, landraces and modern varieties). The genetic diversity analysis revealed significant genome‐wide losses of variation among the three stages and supports a clear distinction between wild and domesticated trees, with only limited gene flow being detected between wild trees and domesticated landraces. We identified 11 domestication sweeps and five breeding sweeps covering, respectively, 11.0 and 2.4 Mb of the P. avium genome. A considerable fraction of the domestication sweeps overlaps with those detected in the related species, Prunus persica (peach), indicating that artificial selection during domestication may have acted independently on the same regions and genes in the two species. We detected 104 candidate genes in sweep regions involved in different processes, such as the determination of fruit texture, the regulation of flowering and fruit ripening and the resistance to pathogens. The signatures of selection identified will enable future evolutionary studies and provide a valuable resource for genetic improvement and conservation programs in sweet cherry.     

Evolution of increased competitiveness in cows trades off with reduced milk yield,fertility and more masculine morphology

In some species females compete for food, foraging territories, mating, and nesting sites. Competing females can exhibit morphological, physiological, and behavioral adaptations typical of males, which are commonly considered as secondary sexual traits. Competition and the development of traits increasing competitiveness require much energy and may exert adverse effects on fecundity and survival. From an evolutionary perspective, positive selection for increased competitiveness would then result in evolution of reduced values for traits related to fitness such as fecundity and survival. There is recent evidence for such evolutionary trade‐offs involving male competition, but no study has considered competing females so far. Using data from competitions for dominance in cows (Bos taurus), we found negative genetic correlations between traits providing success in competition, that is, fighting ability and fitness traits related to milk production and with fertility (the inverse of parity‐conception interval). Fighting ability also showed low but positive genetic correlations with “masculine” morphological traits, and negative correlations with “feminine” traits. A genetic change in traits over time has occurred due to selection on competitiveness, corresponding to an evolutionary process of “masculinization” counteracting the official selection for milk yield. Similar evolutionary trade‐off between success in competition and fitness components may be present in various species experiencing female competition.     

Contrasting Mode of Evolution at a Coat Color Locus in Wild and Domestic Pigs

Despite having only begun ~10,000 years ago, the process of domestication has resulted in a degree of phenotypic variation within individual species normally associated with much deeper evolutionary time scales. Though many variable traits found in domestic animals are the result of relatively recent human-mediated selection, uncertainty remains as to whether the modern ubiquity of long-standing variable traits such as coat color results from selection or drift, and whether the underlying alleles were present in the wild ancestor or appeared after domestication began. Here, through an investigation of sequence diversity at the porcine melanocortin receptor 1 (MC1R) locus, we provide evidence that wild and domestic pig (Sus scrofa) haplotypes from China and Europe are the result of strikingly different selection pressures, and that coat color variation is the result of intentional selection for alleles that appeared after the advent of domestication. Asian and European wild boar (evolutionarily distinct subspecies) differed only by synonymous substitutions, demonstrating that camouflage coat color is maintained by purifying selection. In domestic pigs, however, each of nine unique mutations altered the amino acid sequence thus generating coat color diversity. Most domestic MC1R alleles differed by more than one mutation from the wild-type, implying a long history of strong positive selection for coat color variants, during which time humans have cherry-picked rare mutations that would be quickly eliminated in wild contexts. This pattern demonstrates that coat color phenotypes result from direct human selection and not via a simple relaxation of natural selective pressures.     

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.     

The effect of domestication on some life history traits of sea trout and Atlantic salmon

During the period 1968–1991, certain morphological traits of Atlantic salmon Salmo salar and sea trout S. trutta have been recorded regularly at the hatchery at Älvkarleby, central Sweden. Total body length, weight (for females both before and after stripping), number of eggs, egg size and date of ovulation. A smaller data set for fish marked and released as smolts, providing information about total body length of released smolts, time spent at sea and body size of the recovered adults, was also available for analysis. According to theory and empirical data, the process of artificial breeding results in an evolutionary divergence of the cultured strain from the wild phenotypic norm. The reason for such a divergence is that both natural and sexual selection pressures are altered or relaxed during the process of artificial breeding, as well as random genetic processes, such as founder effects and in- and outbreeding. A path analysis of both species and sexes revealed that the size of the released smolts had increased during the study period. Time spent in sea has decreased for both female and male sea trout, but not for Atlantic salmon. Adult body size for female and male trout have increased as well as female trout condition factor. The increase found in egg size of both species was greater for the salmon than for the trout, indicating that female salmon invest more in egg size with increasing body size. These results support the view that domestication probably has a significant and selective impact on the life history traits of the two salmonid species studied.     

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.     

History, chance and adaptation during biological invasion: separating stochastic phenotypic evolution from response to selection

Introduced species often exhibit changes in genetic variation, population structure, selection regime and phenotypic traits as they colonize and expand into new ranges. For these reasons, species invasions are increasingly recognized as promising systems for studying adaptive evolution over contemporary time scales. However, changes in phenotypic traits during invasion occur under non-equilibrium demographic conditions and may reflect the influences of prior evolutionary history and chance events, as well as selection. We briefly review the evidence for phenotypic evolution and the role of selection during invasion. While there is ample evidence for evolutionary change, it is less clear if selection is the primary mechanism. We then discuss the likelihood that stochastic events shift phenotypic distributions during invasion, and argue that hypotheses of adaptation should be tested against appropriate null models. We suggest two experimental frameworks for separating stochastic evolution from adaptation: statistically accounting for phenotypic variation among putative invasion sources identified by using phylogenetic or assignment methods and by comparing estimates of differentiation within and among ranges for both traits and neutral markers ( Q _ST vs. F _ST). Designs that incorporate a null expectation can reveal the role of history and chance in the evolutionary process, and provide greater insights into evolution during species invasions.     

HOW REPEATABLE IS ADAPTIVE EVOLUTION? THE ROLE OF GEOGRAPHICAL ORIGIN AND FOUNDER EFFECTS IN LABORATORY ADAPTATION

The importance of contingency versus predictability in evolution has been a long-standing issue, particularly the interaction between genetic background, founder effects, and selection. Here we address experimentally the effects of genetic background and founder events on the repeatability of laboratory adaptation in Drosophila subobscura populations for several functional traits. We found disparate starting points for adaptation among laboratory populations derived from independently sampled wild populations for all traits. With respect to the subsequent evolutionary rate during laboratory adaptation, starvation resistance varied considerably among foundations such that the outcome of laboratory evolution is rather unpredictable for this particular trait, even in direction. In contrast, the laboratory evolution of traits closely related to fitness was less contingent on the circumstances of foundation. These findings suggest that the initial laboratory evolution of weakly selected characters may be unpredictable, even when the key adaptations under evolutionary domestication are predictable with respect to their trajectories.     

Plant Domestication and Crop Evolution in the Near East: On Events and Processes

Reconstructing the evolutionary history of crop plants is fundamental for understanding their adaptation profile and the genetic basis of yield-limiting factors, which in turn are critical for future crop improvement. A major topic in this field is the recent claim for a millennia-long ‘protracted’ domestication process. Here we evaluate the evidence for the protracted domestication model in light of published archaeobotanical data, experimental evidence and the biology of the Near Eastern crops and their wild progenitors. The crux of our discussion is the differentiation between events or ‘domestication episodes’ and the later following crop evolutionary processes under domestication (frequently termed ‘crop improvement stage’), which are by definition, still ongoing. We argue that by assuming a protracted millennia-long domestication process, one needlessly opts to operate within an intellectual framework that does not allow differentiating between the decisive (critical) domestication traits and their respective loci, and those that have evolved later during the crop dissemination and improvement following the episodic domestication event. Therefore, in our view, apart from the lack of experimental evidence to support it, the protracted domestication assumption undermines the resolution power of the study of both plant domestication and crop evolution, from the cultural as well as from the biological perspectives.     

Direct and indirect estimates of gene flow among wild and managed populations of Polaskia chichipe, an endemic columnar cactus in Central Mexico

Microsatellite markers were used to obtain direct and indirect estimates of gene flow in populations of Polaskia chichipe under different management regimes, in order to understand the genetic consequences of gene flow in the evolutionary process of domestication. P. chichipe is a columnar cactus endemic to the Tehuacan Valley, Central Mexico, and has come under domestication for its edible fruit. Morphological, phenological, physiological, and reproductive differences, apparently attributable to artificial selection, exist between wild and managed populations, which grow sympatrically. However, strong gene flow may counteract the effects of this selection. In this study, we used paternity analysis to demonstrate that although most of the pollinations occur among individuals within the same population at distances < 40 m, pollen flow from other populations is considerable (27 +/- 5%). Heterogeneity in pollen clouds sampled by mother plants (FST = 0.12) indicated nonrandom mating, which is probably due to temporal heterogeneity in pollen movement. Spatial structure on local and regional scales is consistent with an isolation-by-distance model. The similarity of indirect, direct and demographic estimates of neighbourhood size (74-250 individuals) suggests that this genetic structure is representative of an equilibrium state. These results suggest that traditional management practices have conserved the genetic resources of this species in situ, but also that gene flow is counteracting the effect of domestication to some degree. We discuss our results in the general context of genetic exchange between cultivated and wild populations during the domestication process.     

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.     

Heritability and genetic correlations of fear-related behaviour in Red Junglefowl--possible implications for early domestication

Domesticated species differ from their wild ancestors in a number of traits, generally referred to as the domesticated phenotype. Reduced fear of humans is assumed to have been an early prerequisite for the successful domestication of virtually all species. We hypothesized that fear of humans is linked to other domestication related traits. For three generations, we selected Red Junglefowl (ancestors of domestic chickens) solely on the reaction in a standardized Fear of Human-test. In this, the birds were exposed for a gradually approaching human, and their behaviour was continuously scored. This generated three groups of animals, high (H), low (L) and intermediate (I) fearful birds. The birds in each generation were additionally tested in a battery of behaviour tests, measuring aspects of fearfulness, exploration, and sociality. The results demonstrate that the variation in fear response of Red Junglefowl towards humans has a significant genetic component and is genetically correlated to behavioural responses in other contexts, of which some are associated with fearfulness and others with exploration. Hence, selection of Red Junglefowl on low fear for humans can be expected to lead to a correlated change of other behavioural traits over generations. It is therefore likely that domestication may have caused an initial suite of behavioural modifications, even without selection on anything besides tameness.     

Understanding the establishment success of non-indigenous fishes: lessons from population genetics

During the last 10 years, an increasing number of studies have explored evolutionary aspects of biological invasions. It is becoming increasingly clear that evolutionary processes play an important role during the establishment of non-native species. Genetic drift during the colonization process followed by strong selection imposed through a change in biotic conditions and co-evolutionary disequilibrium set the conditions for rapid evolutionary change in introduced populations. Different hypotheses, which have been proposed to explain how evolutionary and genetic processes, can facilitate invasiveness are explored and their relevance for fish invasions is discussed. Empirical evidence increasingly suggests that admixture after multiple introductions, hybridization between native and non-native species and enemy release can all catalyse the evolution of invasiveness. A number of studies also suggest that genetic bottlenecks might represent less of genetic paradox than previously thought. Much of the theoretical developments and empirical evidence concerning the importance of evolution during biological invasions has been provided from studies on invasive plants. Despite their prominence, fish invasions have received little attention from evolutionary biologists. Recent advances in population genetic analysis such as non-equilibrium methods and genomic techniques such as microarray technology provide suitable tools to address such issues.