MATING SYSTEM,HALDANE'S SIEVE,AND THE DOMESTICATION PROCESS

Mating systems are expected to have a strong influence on both the dynamic of adaptation and the genetic architecture of adaptive traits. In particular, the bias toward the fixation of dominant or partially dominant beneficial mutations predicted under outcrossing (Haldane's sieve) is expected to be reduced under self‐fertilization. To test this prediction in plants, we considered domestication as an example of adaptation. We compiled data from studies reporting the degree of dominance of quantitative trait loci (QTL) involved in the domestication syndrome. We found that adaptation to cultivation mostly proceeded through the selection of recessive and partially recessive genes in predominantly selfing species whereas a much larger fraction of domestication‐related QTL were dominant or partially dominant in outcrossers, as expected under Haldane's sieve. Our study also showed that levels of dominance in mixed mating crop species resemble those observed in selfers, suggesting that recessive alleles can contribute to adaptation even under moderate selfing rates. Although these results rely on a particular example of adaptation, they constitute one of the first attempts to test theoretical expectations on the level of dominance of genes involved in plant adaptation.     

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.     

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.     

A genome‐wide scan for selection signatures in Yorkshire and Landrace pigs based on sequencing data

Pigs have experienced dramatic selection due to domestication, which has led to many different phenotypes when compared to their wild counterparts, especially in the last several decades. Currently, genome‐wide scans in both cattle and humans showing positive selection footprints have been investigated. However, few studies have focused on porcine selection footprints, particularly on a genome‐wide scale. Surveying for selection footprints across porcine genomes can be quite valuable for revealing the genetic mechanisms of phenotypic diversity. Here, we employed a medium sequencing depth (5–20x/site per individual, on average) approach called genotyping by genome reducing and sequencing (GGRS) to detect genome‐wide selection signatures of two domestic pig breeds (Yorkshire and Landrace) that have been under intensive selection for traits of muscle development, growth and behavior. The relative extended haplotype homozygosity test, which identifies selection signatures by measuring the characteristics of haplotypes’ frequency distribution within a single population, was also applied to identify potential positively selected regions. As a result, signatures of positive selection were found in each breed. However, most selection signatures were population specific and related to genomic regions containing genes for biological categories including brain development, metabolism, growth and olfaction. Furthermore, the result of the gene set enrichment analysis indicated that selected regions of the two breeds presented a different over‐representation of genes in the Gene Ontology annotations and Kyoto Encyclopedia of Genes and Genomes pathways. Our results revealed a genome‐wide map of selection footprints in pigs and may help us better understand the mechanisms of selection in pig breeding.     

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.     

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.     

Plant domestication disrupts biodiversity effects across major crop types

Plant diversity fosters productivity in natural ecosystems. Biodiversity effects might increase agricultural yields at no cost in additional inputs. However, the effects of diversity on crop assemblages are inconsistent, probably because crops and wild plants differ in a range of traits relevant to plant–plant interactions. We tested whether domestication has changed the potential of crop mixtures to over‐yield by comparing the performance and traits of major crop species and those of their wild progenitors under varying levels of diversity. We found stronger biodiversity effects in mixtures of wild progenitors, due to larger selection effects. Variation in selection effects was partly explained by within‐mixture differences in leaf size. Our results indicate that domestication might disrupt the ability of crops to benefit from diverse neighbourhoods via reduced trait variance. These results highlight potential limitations of current crop mixtures to over‐yield and the potential of breeding to re‐establish variance and increase mixture performance.     

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.     

SIGNALING EFFICACY DRIVES THE EVOLUTION OF LARGER SEXUAL ORNAMENTS BY SEXUAL SELECTION

Why are there so few small secondary sexual characters? Theoretical models predict that sexual selection should lead to reduction as often as exaggeration, and yet we mainly associate secondary sexual ornaments with exaggerated features such as the peacock's tail. We review the literature on mate choice experiments for evidence of reduced sexual traits. This shows that reduced ornamentation is effectively impossible in certain types of ornamental traits (behavioral, pheromonal, or color‐based traits, and morphological ornaments for which the natural selection optimum is no trait), but that there are many examples of morphological traits that would permit reduction. Yet small sexual traits are very rarely seen. We analyze a simple mathematical model of Fisher's runaway process (the null model for sexual selection). Our analysis shows that the imbalance cannot be wholly explained by larger ornaments being less costly than smaller ornaments, nor by preferences for larger ornaments being less costly than preferences for smaller ornaments. Instead, we suggest that asymmetry in signaling efficacy limits runaway to trait exaggeration.     

Mutualism breakdown in breadfruit domestication

During the process of plant domestication, below-ground communities are rarely considered. Some studies have attempted to understand the changes in root symbionts owing to domestication, but little is known about how it influences mycorrhizal response in domesticated crops. We hypothesized that selection for above-ground traits may also result in decreased mycorrhizal abundance in roots. Breadfruit (Artocarpus sp.) has a long domestication history, with a strong geographical movement of cultivars from west to east across the Melanesian and Polynesian islands. Our results clearly show a decrease in arbuscular mycorrhizas (AMs) along a domestication gradient from wild to recently derived cultivars. We showed that the vesicular and arbuscular colonization rate decreased significantly in more recently derived breadfruit cultivars. In addition, molecular analyses of breadfruit roots indicated that AM fungal species richness also responded along the domestication gradient. These results suggest that human-driven selection for plant cultivars can have unintended effects on below-ground mutualists, with potential impacts on the stress tolerance of crops and long-term food security.     

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.     

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.     

Is sexual selection driving diversification of the bioluminescent ponyfishes (Teleostei: Leiognathidae)?

Sexual selection may facilitate genetic isolation among populations and result in increased rates of diversification. As a mechanism driving diversification, sexual selection has been invoked and upheld in numerous empirical studies across disparate taxa, including birds, plants and spiders. In this study, we investigate the potential impact of sexual selection on the tempo and mode of ponyfish evolution. Ponyfishes (Leiognathidae) are bioluminescent marine fishes that exhibit sexually dimorphic features of their unique light-organ system (LOS). Although sexual selection is widely considered to be the driving force behind ponyfish speciation, this hypothesis has never been formally tested. Given that some leiognathid species have a sexually dimorphic LOS, whereas others do not, this family provides an excellent system within which to study the potential role of sexual selection in diversification and morphological differentiation. In this study, we estimate the phylogenetic relationships and divergence times for Leiognathidae, investigate the tempo and mode of ponyfish diversification, and explore morphological shape disparity among leiognathid clades. We recover strong support for a monophyletic Leiognathidae and estimate that all major ponyfish lineages evolved during the Paleogene. Our studies of ponyfish diversification demonstrate that there is no conclusive evidence that sexually dimorphic clades are significantly more species rich than nonsexually dimorphic lineages and that evidence is lacking to support any significant diversification rate increases within ponyfishes. Further, we detected a lineage-through-time signal indicating that ponyfishes have continuously diversified through time, which is in contrast to many recent diversification studies that identify lineage-through-time patterns that support mechanisms of density-dependent speciation. Additionally, there is no evidence of sexual selection hindering morphological diversity, as sexually dimorphic taxa are shown to be more disparate in overall shape morphology than nonsexually dimorphic taxa. Our results suggest that if sexual selection is occurring in ponyfish evolution, it is likely acting only as a genetic isolating mechanism that has allowed ponyfishes to continuously diversify over time, with no overall impact on increases in diversification rate or morphological disparity.     

A guinea fowl genome assembly provides new evidence on evolution following domestication and selection in galliformes

The helmeted guinea fowl Numida meleagris belongs to the order Galliformes. Its natural range includes a large part of sub‐Saharan Africa, from Senegal to Eritrea and from Chad to South Africa. Archaeozoological and artistic evidence suggest domestication of this species may have occurred about 2,000 years BP in Mali and Sudan primarily as a food resource, although villagers also benefit from its capacity to give loud alarm calls in case of danger, of its ability to consume parasites such as ticks and to hunt snakes, thus suggesting its domestication may have resulted from a commensal association process. Today, it is still farmed in Africa, mainly as a traditional village poultry, and is also bred more intensively in other countries, mainly France and Italy. The lack of available molecular genetic markers has limited the genetic studies conducted to date on guinea fowl. We present here a first‐generation whole‐genome sequence draft assembly used as a reference for a study by a Pool‐seq approach of wild and domestic populations from Europe and Africa. We show that the domestic populations share a higher genetic similarity between each other than they do to wild populations living in the same geographical area. Several genomic regions showing selection signatures putatively related to domestication or importation to Europe were detected, containing candidate genes, most notably EDNRB2, possibly explaining losses in plumage coloration phenotypes in domesticated populations.     

The role of Bh4 in parallel evolution of hull colour in domesticated and weedy rice

The two independent domestication events in the genus Oryza that led to African and Asian rice offer an extremely useful system for studying the genetic basis of parallel evolution. This system is also characterized by parallel de‐domestication events, with two genetically distinct weedy rice biotypes in the US derived from the Asian domesticate. One important trait that has been altered by rice domestication and de‐domestication is hull colour. The wild progenitors of the two cultivated rice species have predominantly black‐coloured hulls, as does one of the two U.S. weed biotypes; both cultivated species and one of the US weedy biotypes are characterized by straw‐coloured hulls. Using Black hull 4 (Bh4) as a hull colour candidate gene, we examined DNA sequence variation at this locus to study the parallel evolution of hull colour variation in the domesticated and weedy rice system. We find that independent Bh4‐coding mutations have arisen in African and Asian rice that are correlated with the straw hull phenotype, suggesting that the same gene is responsible for parallel trait evolution. For the U.S. weeds, Bh4 haplotype sequences support current hypotheses on the phylogenetic relationship between the two biotypes and domesticated Asian rice; straw hull weeds are most similar to indica crops, and black hull weeds are most similar to aus crops. Tests for selection indicate that Asian crops and straw hull weeds deviate from neutrality at this gene, suggesting possible selection on Bh4 during both rice domestication and de‐domestication.     

Lack of low frequency variants masks patterns of non-neutral evolution following domestication

Detecting artificial selection in the genome of domesticated species can not only shed light on human history but can also be beneficial to future breeding strategies. Evidence for selection has been documented in domesticated species including maize and rice, but few studies have to date detected signals of artificial selection in the Sorghum bicolor genome. Based on evidence that domesticated S. bicolor and its wild relatives show significant differences in endosperm structure and quality, we sequenced three candidate seed storage protein (kafirin) loci and three candidate starch biosynthesis loci to test whether these genes show non-neutral evolution resulting from the domestication process. We found strong evidence of non-neutral selection at the starch synthase IIa gene, while both starch branching enzyme I and the beta kafirin gene showed weaker evidence of non-neutral selection. We argue that the power to detect consistent signals of non-neutral selection in our dataset is confounded by the absence of low frequency variants at four of the six candidate genes. A future challenge in the detection of positive selection associated with domestication in sorghum is to develop models that can accommodate for skewed frequency spectrums.     

Genomic screening for artificial selection during domestication and improvement in maize

BACKGROUND: Artificial selection results in phenotypic evolution. Maize (Zea mays L. ssp. mays) was domesticated from its wild progenitor teosinte (Zea mays subspecies parviglumis) through a single domestication event in southern Mexico between 6000 and 9000 years ago. This domestication event resulted in the original maize landrace varieties. The landraces provided the genetic material for modern plant breeders to select improved varieties and inbred lines by enhancing traits controlling agricultural productivity and performance. Artificial selection during domestication and crop improvement involved selection of specific alleles at genes controlling key morphological and agronomic traits, resulting in reduced genetic diversity relative to unselected genes. SCOPE: This review is a summary of research on the identification and characterization by population genetics approaches of genes affected by artificial selection in maize. CONCLUSIONS: Analysis of DNA sequence diversity at a large number of genes in a sample of teosintes and maize inbred lines indicated that approx. 2 % of maize genes exhibit evidence of artificial selection. The remaining genes give evidence of a population bottleneck associated with domestication and crop improvement. In a second study to efficiently identify selected genes, the genes with zero sequence diversity in maize inbreds were chosen as potential targets of selection and sequenced in diverse maize landraces and teosintes, resulting in about half of candidate genes exhibiting evidence for artificial selection. Extended gene sequencing demonstrated a low false-positive rate in the approach. The selected genes have functions consistent with agronomic selection for plant growth, nutritional quality and maturity. Large-scale screening for artificial selection allows identification of genes of potential agronomic importance even when gene function and the phenotype of interest are unknown. These approaches should also be applicable to other domesticated species if specific demographic conditions during domestication exist.     

A large-scale screen for artificial selection in maize identifies candidate agronomic loci for domestication and crop improvement

Maize (Zea mays subsp mays) was domesticated from teosinte (Z. mays subsp parviglumis) through a single domestication event in southern Mexico between 6000 and 9000 years ago. This domestication event resulted in the original maize landrace varieties, which were spread throughout the Americas by Native Americans and adapted to a wide range of environmental conditions. Starting with landraces, 20th century plant breeders selected inbred lines of maize for use in hybrid maize production. Both domestication and crop improvement involved selection of specific alleles at genes controlling key morphological and agronomic traits, resulting in reduced genetic diversity relative to unselected genes. Here, we sequenced 1095 maize genes from a sample of 14 inbred lines and chose 35 genes with zero sequence diversity as potential targets of selection. These 35 genes were then sequenced in a sample of diverse maize landraces and teosintes and tested for selection. Using two statistical tests, we identified eight candidate genes. Extended gene sequencing of these eight candidate loci confirmed that six were selected throughout the gene, and the remaining two exhibited evidence of selection in the 3' portion of each gene. The selected genes have functions consistent with agronomic selection for nutritional quality, maturity, and productivity. Our large-scale screen for artificial selection allows identification of genes of potential agronomic importance even when gene function and the phenotype of interest are unknown.