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A wide diversity of mating systems occur in nature, with frequent evolutionary transitions in mating-compatibility mechanisms. Basidiomycete fungi typically have two mating-type loci controlling mating compatibility, HD and PR, usually residing on different chromosomes. In Microbotryum anther-smut fungi, there have been repeated events of linkage between the two mating-type loci through chromosome fusions, leading to large non-recombining regions. By generating high-quality genome assemblies, we found that two sister Microbotryum species parasitizing Dianthus plants, M. superbum and M. shykoffianum, as well as the distantly related M. scorzonarae, have their HD and PR mating-type loci on different chromosomes, but with the PR mating-type chromosome fused with part of the ancestral HD chromosome. Furthermore, progressive extensions of recombination suppression have generated evolutionary strata. In all three species, rearrangements suggest the existence of a transient stage of HD-PR linkage by whole chromosome fusion, and, unexpectedly, the HD genes lost their function. In M. superbum, multiple natural diploid strains were homozygous, and the disrupted HD2 gene was hardly expressed. Mating tests confirmed that a single genetic factor controlled mating compatibility (i.e. PR) and that haploid strains with identical HD alleles could mate and produce infectious hyphae. The HD genes have therefore lost their function in the control of mating compatibility in these Microbotryum species. While the loss of function of PR genes in mating compatibility has been reported in a few basidiomycete fungi, these are the first documented cases for the loss of mating-type determination by HD genes in heterothallic fungi. The control of mating compatibility by a single genetic factor is beneficial under selfing and can thus be achieved repeatedly, through evolutionary convergence in distant lineages, involving different genomic or similar pathways.
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The domestication process in long-lived plant perennials differs dramatically from that of annuals, with a huge amount of genetic exchange between crop and wild populations. Though apple is a major fruit crop grown worldwide, the contribution of wild apple species to the genetic makeup of the cultivated apple genome remains a topic of intense study. We used population genomics approaches to investigate the contributions of several wild apple species to European and Chinese rootstock and dessert genomes, with a focus on the extent of wild-crop gene flow. Population genetic structure inferences revealed that the East Asian wild apples, Malus baccata (L.) Borkh and M. hupehensis (Pamp.), form a single panmictic group, and that the European dessert and rootstock apples form a specific gene pool whereas the Chinese dessert and rootstock apples were a mixture of three wild gene pools, suggesting different evolutionary histories of European and Chinese apple varieties. Coalescent-based inferences and gene flow estimates indicated that M. baccata - M. hupehensis contributed to the genome of both European and Chinese cultivated apples through wild-to-crop introgressions, and not as an initial contributor as previously supposed. We also confirmed the contribution through wild-to-crop introgressions of Malus sylvestris Mill. to the cultivated apple genome. Apple tree domestication is therefore one example in woody perennials that involved gene flow from several wild species from multiple geographical areas. This study provides an example of a complex protracted process of domestication in long-lived plant perennials, and is a starting point for apple breeding programmes.
Asunto(s)
Malus , Evolución Biológica , Frutas/genética , Malus/genética , Fitomejoramiento , Pool de GenesRESUMEN
Divergence processes in crop-wild fruit tree complexes in pivotal regions for plant domestication such as the Caucasus and Iran remain little studied. We investigated anthropogenic and natural divergence processes in apples in these regions using 26 microsatellite markers amplified in 550 wild and cultivated samples. We found two genetically distinct cultivated populations in Iran that are differentiated from Malus domestica, the standard cultivated apple worldwide. Coalescent-based inferences showed that these two cultivated populations originated from specific domestication events of Malus orientalis in Iran. We found evidence of substantial wild-crop and crop-crop gene flow in the Caucasus and Iran, as has been described in apple in Europe. In addition, we identified seven genetically differentiated populations of wild apple (M. orientalis), not introgressed by the cultivated apple. Niche modelling combined with genetic diversity estimates indicated that these wild populations likely resulted from range changes during past glaciations. This study identifies Iran as a key region in the domestication of apple and M. orientalis as an additional contributor to the cultivated apple gene pool. Domestication of the apple tree therefore involved multiple origins of domestication in different geographic locations and substantial crop-wild hybridization, as found in other fruit trees. This study also highlights the impact of climate change on the natural divergence of a wild fruit tree and provides a starting point for apple conservation and breeding programmes in the Caucasus and Iran.
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Malus , Malus/genética , Domesticación , Pool de Genes , Irán , FitomejoramientoRESUMEN
The colonization success of a species depends on the interplay between its phenotypic plasticity, adaptive potential and demographic history. Assessing their relative contributions during the different phases of a species range expansion is challenging, and requires large-scale experiments. Here, we investigated the relative contributions of plasticity, performance and demographic history to the worldwide expansion of the shepherd's purse, Capsella bursa-pastoris. We installed two large common gardens of the shepherd's purse, a young, self-fertilizing, allopolyploid weed with a worldwide distribution. One common garden was located in Europe, the other in Asia. We used accessions from three distinct genetic clusters (Middle East, Europe and Asia) that reflect the demographic history of the species. Several life-history traits were measured. To explain the phenotypic variation between and within genetic clusters, we analysed the effects of (i) the genetic clusters, (ii) the phenotypic plasticity and its association to fitness and (iii) the distance in terms of bioclimatic variables between the sampling site of an accession and the common garden, i.e. the environmental distance. Our experiment showed that (i) the performance of C. bursa-pastoris is closely related to its high phenotypic plasticity; (ii) within a common garden, genetic cluster was a main determinant of phenotypic differences; and (iii) at the scale of the experiment, the effect of environmental distance to the common garden could not be distinguished from that of genetic clusters. Phenotypic plasticity and demographic history both play important role at different stages of range expansion. The success of the worldwide expansion of C. bursa-pastoris was undoubtedly influenced by its strong phenotypic plasticity.
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Fruit maturation and softening are critical traits that control fruit shelf-life. In the climacteric tomato (Solanum lycopersicum L.) fruit, ethylene plays a key role in fruit ripening and softening. We characterized two related proteins with contrasting impact on ethylene production, ACC oxidase 1 (SlACO1) and SlE8. We found SlACO1 and SlE8 to be highly expressed during fruit ripening. To identify loss-of-function alleles, we analysed the tomato genetic diversity but we did not find any natural mutations impairing the function of these proteins. We also found the two loci evolving under purifying selection. To engineer hypomorphic alleles, we used TILLING (target-induced local lesions in genomes) to screen a tomato ethylmethane sulfonate-mutagenized population. We found 13 mutants that we phenotyped for ethylene production, shelf-life, firmness, conductivity, and soluble solid content in tomato fruits. The data demonstrated that slaco1-1 and slaco1-2 alleles could be used to improve fruit shelf-life, and that sle8-1 and sle8-2 alleles could be used to accelerate ripening. This study highlights further the importance of SlACO1 and SlE8 in ethylene production in tomato fruit and how they might be used for post-harvest fruit preservation or speeding up fruit maturation.
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Solanum lycopersicum , Etilenos , Frutas/genética , Frutas/metabolismo , Regulación de la Expresión Génica de las Plantas , Solanum lycopersicum/genética , Solanum lycopersicum/metabolismo , Mutación , Fenotipo , Proteínas de Plantas/genética , Proteínas de Plantas/metabolismoRESUMEN
A road-map of the genetic and phenotypic diversities in both crops and their wild related species can help identifying valuable genetic resources for further crop breeding. The clary sage (Salvia sclarea L.), a perfume, medicinal and aromatic plant, is used for sclareol production and ornamental purposes. Despite its wide use in the field of cosmetics, the phenotypic and genetic diversity of wild and cultivated clary sages remains to be explored. We characterized the genetic and phenotypic variation of a collection of six wild S. sclarea populations from Croatia, sampled along an altitudinal gradient, and, of populations of three S. sclarea cultivars. We showed low level of genetic diversity for the two S. sclarea traditional cultivars used for essential oil production and for ornamental purposes, respectively. In contrast, a recent cultivar resulting from new breeding methods, which involve hybridizations among several genotypes rather than traditional recurrent selection and self-crosses over time, showed high genetic diversity. We also observed a marked phenotypic differentiation for the ornamental clary sage compared with other cultivated and wild clary sages. Instead, the two cultivars used for essential oil production, a traditional and a recent one, respectively, were not phenotypically differentiated from the wild Croatian populations. Our results also featured some wild populations with high sclareol content and early-flowering phenotypes as good candidates for future breeding programs. This study opens up perspectives for basic research aiming at understanding the impact of breeding methods on clary sage evolution, and highlights interesting avenues for clary breeding programs.
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Variación Biológica Poblacional , Variación Genética , Perfumes , Fitomejoramiento , Salvia/genética , Aceites VolátilesRESUMEN
Among crop fruit trees, the apricot (Prunus armeniaca) provides an excellent model to study divergence and adaptation processes. Here, we obtain nearly 600 Armeniaca apricot genomes and four high-quality assemblies anchored on genetic maps. Chinese and European apricots form two differentiated gene pools with high genetic diversity, resulting from independent domestication events from distinct wild Central Asian populations, and with subsequent gene flow. A relatively low proportion of the genome is affected by selection. Different genomic regions show footprints of selection in European and Chinese cultivated apricots, despite convergent phenotypic traits, with predicted functions in both groups involved in the perennial life cycle, fruit quality and disease resistance. Selection footprints appear more abundant in European apricots, with a hotspot on chromosome 4, while admixture is more pervasive in Chinese cultivated apricots. Our study provides clues to the biology of selected traits and targets for fruit tree research and breeding.
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Domesticación , Genoma de Planta/genética , Prunus armeniaca/genética , Cromosomas de las Plantas/genética , Resistencia a la Enfermedad/genética , Evolución Molecular , Frutas/clasificación , Frutas/genética , Frutas/crecimiento & desarrollo , Flujo Génico , Variación Genética , Estadios del Ciclo de Vida/genética , Metagenómica , Fenotipo , Filogenia , Prunus armeniaca/clasificación , Prunus armeniaca/crecimiento & desarrollo , Selección GenéticaRESUMEN
Host-parasite coevolution is ubiquitous, shaping genetic and phenotypic diversity and the evolutionary trajectory of interacting species. With the advances of high throughput sequencing technologies applicable to model and non-model organisms alike, it is now feasible to study in greater detail (a) the genetic underpinnings of coevolution, (b) the speed and type of dynamics at coevolving loci, and (c) the genomic consequences of coevolution. This review focuses on three recently developed approaches that leverage information from host and parasite full genome data simultaneously to pinpoint coevolving loci and draw inference on the coevolutionary history. First, co-genome-wide association study (co-GWAS) methods allow pinpointing the loci underlying host-parasite interactions. These methods focus on detecting associations between genetic variants and the outcome of experimental infection tests or on correlations between genomes of naturally infected hosts and their infecting parasites. Second, extensions to population genomics methods can detect genes under coevolution and infer the coevolutionary history, such as fitness costs. Third, correlations between host and parasite population size in time are indicative of coevolution, and polymorphism levels across independent spatially distributed populations of hosts and parasites can reveal coevolutionary loci and infer coevolutionary history. We describe the principles of these three approaches and discuss their advantages and limitations based on coevolutionary theory. We present recommendations for their application to various host (prokaryotes, fungi, plants, and animals) and parasite (viruses, bacteria, fungi, and macroparasites) species. We conclude by pointing out methodological and theoretical gaps to be filled to extract maximum information from full genome data and thereby to shed light on the molecular underpinnings of coevolution.
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Parásitos , Animales , Evolución Biológica , Estudio de Asociación del Genoma Completo , Genómica , Interacciones Huésped-Parásitos/genética , Parásitos/genéticaRESUMEN
Reproductive strategies play a major role in plant speciation. Notably, transitions from outcrossing to selfing may lead to relaxed sexual selection and parental conflict. Shifts in mating systems can affect maternal and paternal interests, and thus parent-specific influence on endosperm development, leading to reproductive isolation: if selfing and outcrossing species hybridize, the resulting seeds may not be viable due to endosperm failure. Nevertheless, it remains unclear how the switch in mating systems can impact reproductive isolation between recently diverged lineages, that is, during the process of speciation. We investigated this question using Arabidopsis lyrata, which recently transitioned to selfing (10,000 years ago) in certain North American populations, where European populations remain outcrossing. We performed reciprocal crosses between selfers and outcrossers, and measured seed viability and endosperm development. We show that parental genomes in the hybrid seed negatively interact, as predicted by parental conflict. This leads to extensive hybrid seed lethality associated with endosperm cellularization disturbance. Our results suggest that this is primarily driven by divergent evolution of the paternal genome between selfers and outcrossers. In addition, we observed other hybrid seed defects, suggesting that sex-specific interests are not the only processes contributing to postzygotic reproductive isolation.
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Arabidopsis/genética , Hibridación Genética , Aislamiento Reproductivo , Arabidopsis/fisiología , Cruzamientos Genéticos , Endospermo/genética , Fenotipo , ReproducciónRESUMEN
The European crabapple Malus sylvestris, a crop wild relative of Malus domestica, is a major contributor to the cultivated apple genome and represents a potential source of interesting alleles or genes, particularly pest resistance traits. An original approach was used to explore the trophic interaction between M. sylvestris populations and its pest, the rosy apple aphid (Dysaphis plantaginea). Using 13 microsatellite markers, population genetic structure and level of crop-to-wild introgressions were inferred between M. sylvestris seedlings from three sites in Europe (Denmark, France, Romania), and M. domestica seedlings. Genetically characterized plants were also used to analyze aphid feeding behavior and fitness parameters. First, aphids submitted to two genetically close M. sylvestris populations (the Danish and French) exhibited similar behavioral parameters, suggesting similar patterns of resistance in these host plants. Second, the Romanian M. sylvestris population was most closely genetically related to M. domestica. Although the two plant genetic backgrounds were significantly differentiated, they showed comparable levels of sensitivity to D. plantaginea infestation. Third, aphid fitness parameters were not significantly impacted by the host plant's genetic background. Finally, crop-to-wild introgression seemed to significantly drive resistance to D. plantaginea independent of host plant population genetic structure, with hybrids being less suitable hosts.
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Áfidos/fisiología , Malus/genética , Malus/parasitología , Animales , Conducta Alimentaria , Interacciones Huésped-Parásitos , Hibridación Genética , Dinámica Poblacional , Plantones/genéticaRESUMEN
Since Darwin's time, the role of crop wild relatives (CWR), landraces, and cultivated genepools in shaping plant diversity and boosting food resources has been a major question [...].
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Productos Agrícolas/genética , Evolución Molecular , Plantas/genética , Flujo Génico , Genes de Plantas , Hibridación Genética , Estrés Fisiológico/genéticaRESUMEN
Study of the congruence of population genetic structure between hosts and pathogens gives important insights into their shared phylogeographical and coevolutionary histories. We studied the population genetic structure of castrating anther-smut fungi (genus Microbotryum) and of their host plants, the Silene nutans species complex, and the morphologically and genetically closely related Silene italica, which can be found in sympatry. Phylogeographical population genetic structure related to persistence in separate glacial refugia has been recently revealed in the S. nutans plant species complex across Western Europe, identifying several distinct lineages. We genotyped 171 associated plant-pathogen pairs of anther-smut fungi and their host plant individuals using microsatellite markers and plant chloroplastic single nucleotide polymorphisms. We found clear differentiation between fungal populations parasitizing S. nutans and S. italica plants. The population genetic structure of fungal strains parasitizing the S. nutans plant species complex mirrored the host plant genetic structure, suggesting that the pathogen was isolated in glacial refugia together with its host and/or that it has specialized on the plant genetic lineages. Using random forest approximate Bayesian computation (ABC-RF), we found that the divergence history of the fungal lineages on S. nutans was congruent with that previously inferred for the host plant and probably occurred with ancient but no recent gene flow. Genome sequences confirmed the genetic structure and the absence of recent gene flow between fungal genetic lineages. Our analyses of individual host-pathogen pairs contribute to a better understanding of co-evolutionary histories between hosts and pathogens in natural ecosystems, in which such studies remain scarce.
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Basidiomycota/genética , Coevolución Biológica , Genética de Población , Silene/genética , Silene/microbiología , Núcleo Celular/genética , ADN de Cloroplastos/genética , Europa (Continente) , Flores/microbiología , Flujo Génico , Marcadores Genéticos , Genoma Fúngico , Genoma de Planta , Genotipo , Repeticiones de Microsatélite , Filogeografía , Enfermedades de las Plantas/microbiología , Polimorfismo de Nucleótido Simple , Silene/clasificaciónRESUMEN
Domestication is an excellent model to study diversification and this evolutionary process can be different in perennial plants, such as fruit trees, compared to annual crops. Here, we inferred the history of wild apricot species divergence and of apricot domestication history across Eurasia, with a special focus on Central and Eastern Asia, based on microsatellite markers and approximate Bayesian computation. We significantly extended our previous sampling of apricots in Europe and Central Asia towards Eastern Asia, resulting in a total sample of 271 cultivated samples and 306 wild apricots across Eurasia, mainly Prunus armeniaca and Prunus sibirica, with some Prunus mume and Prunus mandshurica. We recovered wild Chinese species as genetically differentiated clusters, with P. sibirica being divided into two clusters, one possibly resulting from hybridization with P. armeniaca. Central Asia also appeared as a diversification centre of wild apricots. We further revealed at least three domestication events, without bottlenecks, that gave rise to European, Southern Central Asian and Chinese cultivated apricots, with ancient gene flow among them. The domestication event in China possibly resulted from ancient hybridization between wild populations from Central and Eastern Asia. We also detected extensive footprints of recent admixture in all groups of cultivated apricots. Our results thus show that apricot is an excellent model for studying speciation and domestication in long-lived perennial fruit trees.
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Domesticación , Frutas/genética , Variación Genética/genética , Prunus armeniaca/genética , China , Europa (Continente) , Evolución Molecular , Frutas/crecimiento & desarrollo , Flujo Génico/genética , Hibridación Genética , Especificidad de la EspecieRESUMEN
The apple is an iconic tree and a major fruit crop worldwide. It is also a model species for the study of the evolutionary processes and genomic basis underlying the domestication of clonally propagated perennial crops. Multidisciplinary approaches from across Eurasia have documented the pace and process of cultivation of this remarkable crop. While population genetics and genomics have revealed the overall domestication history of apple across Eurasia, untangling the evolutionary processes involved, archeobotany has helped to document the transition from gathering and using apples to the practice of cultivation. Further studies integrating archeogenetic and archeogenomic approaches will bring new insights about key traits involved in apple domestication. Such knowledge has potential to boost innovation in present-day apple breeding.
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Malus , Cruzamiento , Productos Agrícolas , Domesticación , FrutasRESUMEN
Anther-smut fungi provide a powerful system to study host-pathogen specialization and coevolution, with hundreds of Microbotryum species specialized on diverse Caryophyllaceae plants, castrating their hosts through manipulation of the hosts' reproductive organs to facilitate disease transmission. Microbotryum fungi have exceptional genomic characteristics, including dimorphic mating-type chromosomes, that make this genus anexcellent model for studying the evolution of mating systems and their influence on population genetics structure and adaptive potential. Important insights into adaptation, coevolution, host specialization, and mating system evolution have been gained using anther-smut fungi, with new insights made possible by the recent advent of genomic approaches. We illustrate with Microbotryum case studies how using a combination of comparative genomics, population genomics, and transcriptomics approaches enables the integration of different evolutionary perspectives across different timescales. We also highlight current challenges and suggest future studies that will contribute to advancing our understanding of the mechanisms underlying adaptive processes in populations of fungal pathogens.
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Basidiomycota , Adaptación Fisiológica , Hongos , Genómica , PlantasRESUMEN
In 2010, a major scientific milestone was achieved for tree fruit crops: publication of the first draft whole genome sequence (WGS) for apple (Malus domestica). This WGS, v1.0, was valuable as the initial reference for sequence information, fine mapping, gene discovery, variant discovery, and tool development. A new, high quality apple WGS, GDDH13 v1.1, was released in 2017 and now serves as the reference genome for apple. Over the past decade, these apple WGSs have had an enormous impact on our understanding of apple biological functioning, trait physiology and inheritance, leading to practical applications for improving this highly valued crop. Causal gene identities for phenotypes of fundamental and practical interest can today be discovered much more rapidly. Genome-wide polymorphisms at high genetic resolution are screened efficiently over hundreds to thousands of individuals with new insights into genetic relationships and pedigrees. High-density genetic maps are constructed efficiently and quantitative trait loci for valuable traits are readily associated with positional candidate genes and/or converted into diagnostic tests for breeders. We understand the species, geographical, and genomic origins of domesticated apple more precisely, as well as its relationship to wild relatives. The WGS has turbo-charged application of these classical research steps to crop improvement and drives innovative methods to achieve more durable, environmentally sound, productive, and consumer-desirable apple production. This review includes examples of basic and practical breakthroughs and challenges in using the apple WGSs. Recommendations for "what's next" focus on necessary upgrades to the genome sequence data pool, as well as for use of the data, to reach new frontiers in genomics-based scientific understanding of apple.
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Hybrid seed lethality is a widespread type of reproductive barrier among angiosperm taxa1,2 that contributes to species divergence by preventing gene flow between natural populations3,4. Besides its ecological importance, it is an important obstacle to plant breeding strategies 5 . Hybrid seed lethality is mostly due to a failure of the nourishing endosperm tissue, resulting in embryo arrest3,6,7. The cause of this failure is a parental dosage imbalance in the endosperm that can be a consequence of either differences in parental ploidy levels or differences in the 'effective ploidy', also known as the endosperm balance number (EBN)8,9. Hybrid seed defects exhibit a parent-of-origin pattern3,6,7, suggesting that differences in number or expression strength of parent-of-origin-specific imprinted genes underpin, as the primary or the secondary cause, the molecular basis of the EBN7,10. Here, we have tested this concept in the genus Capsella and show that the effective ploidy of three Capsella species correlates with the number and expression level of paternally expressed genes (PEGs). Importantly, the number of PEGs and the effective ploidy decrease with the selfing history of a species: the obligate outbreeder Capsella grandiflora had the highest effective ploidy, followed by the recent selfer Capsella rubella and the ancient selfer Capsella orientalis. PEGs were associated with the presence of transposable elements and their silencing mark, DNA methylation in CHH context (where H denotes any base except C). This suggests that transposable elements have driven the imprintome divergence between Capsella species. Together, we propose that variation in transposable element insertions, the resulting differences in PEG number and divergence in their expression level form one component of the effective ploidy variation between species of different breeding system histories, and, as a consequence, allow the establishment of endosperm-based hybridization barriers.
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Capsella/genética , Genes de Plantas/genética , Impresión Genómica/genética , Aislamiento Reproductivo , Metilación de ADN , Elementos Transponibles de ADN/genética , ADN de Plantas/genética , Diploidia , Endospermo/metabolismo , Regulación de la Expresión Génica de las Plantas/genética , PloidiasRESUMEN
Background: Unravelling domestication processes is crucial for understanding how species respond to anthropogenic pressures, forecasting crop responses to future global changes and improving breeding programmes. Domestication processes for clonally propagated perennials differ markedly from those for seed-propagated annual crops, mostly due to long generation times, clonal propagation and recurrent admixture with local forms, leading to a limited number of generations of selection from wild ancestors. However, additional case studies are required to document this process more fully. Scope: The olive is an iconic species in Mediterranean cultural history. Its multiple uses and omnipresence in traditional agrosystems have made this species an economic pillar and cornerstone of Mediterranean agriculture. However, major questions about the domestication history of the olive remain unanswered. New paleobotanical, archeological, historical and molecular data have recently accumulated for olive, making it timely to carry out a critical re-evaluation of the biogeography of wild olives and the history of their cultivation. We review here the chronological history of wild olives and discuss the questions that remain unanswered, or even unasked, about their domestication history in the Mediterranean Basin. We argue that more detailed ecological genomics studies of wild and cultivated olives are crucial to improve our understanding of olive domestication. Multidisciplinary research integrating genomics, metagenomics and community ecology will make it possible to decipher the evolutionary ecology of one of the most iconic domesticated fruit trees worldwide. Conclusion: The olive is a relevant model for improving our knowledge of domestication processes in clonally propagated perennial crops, particularly those of the Mediterranean Basin. Future studies on the ecological and genomic shifts linked to domestication in olive and its associated community will provide insight into the phenotypic and molecular bases of crop adaptation to human uses.