Genetic diversity, gene flow, and differentiation among wild, semiwild, and landrace chile pepper (Capsicum annuum) populations in Oaxaca, Mexico.

PREMISE: Capsicum annuum (Solanaceae) was originally domesticated in Mexico, where wild (C. annuum var. glabriusculum) and cultivated (C. annuum var. annuum) chile pepper populations (>60 landraces) are common, and wild-resembling individuals (hereafter semiwild) grow spontaneously in anthropogenic environments. Here we analyze the role of elevation and domestication gradients in shaping the genetic diversity in C. annuum from the state of Oaxaca, Mexico. METHODS: We collected samples of 341 individuals from 28 populations, corresponding to wild, semiwild (C. annuum var. glabriusculum) and cultivated C. annuum, and closely related species Capsicum frutescens and C. chinense. From the genetic variation of 10 simple sequence repeat (SSR) loci, we assessed the population genetic structure, inbreeding, and gene flow through variance distribution analyses, genetic clustering, and connectivity estimations. RESULTS: Genetic diversity (HE ) did not differ across domestication levels. However, inbreeding coefficients were higher in semiwild and cultivated chiles than in wild populations. We found evidence for gene flow between wild populations and cultivated landraces along the coast. Genetic structure analysis revealed strong differentiation between most highland and lowland landraces. CONCLUSIONS: Gene flow between wild and domesticated populations may be mediated by backyards and smallholder farms, while mating systems may facilitate gene flow between landraces and semiwild populations. Domestication and elevation may overlap in their influence on genetic differentiation. Lowland Gui'ña dani clustered with highland landraces perhaps due to the social history of the Zapotec peoples. In situ conservation may play an important role in preserving semiwild populations and private alleles found in landraces.

Common gardens in teosintes reveal the establishment of a syndrome of adaptation to altitude.

In plants, local adaptation across species range is frequent. Yet, much has to be discovered on its environmental drivers, the underlying functional traits and their molecular determinants. Genome scans are popular to uncover outlier loci potentially involved in the genetic architecture of local adaptation, however links between outliers and phenotypic variation are rarely addressed. Here we focused on adaptation of teosinte populations along two elevation gradients in Mexico that display continuous environmental changes at a short geographical scale. We used two common gardens, and phenotyped 18 traits in 1664 plants from 11 populations of annual teosintes. In parallel, we genotyped these plants for 38 microsatellite markers as well as for 171 outlier single nucleotide polymorphisms (SNPs) that displayed excess of allele differentiation between pairs of lowland and highland populations and/or correlation with environmental variables. Our results revealed that phenotypic differentiation at 10 out of the 18 traits was driven by local selection. Trait covariation along the elevation gradient indicated that adaptation to altitude results from the assembly of multiple co-adapted traits into a complex syndrome: as elevation increases, plants flower earlier, produce less tillers, display lower stomata density and carry larger, longer and heavier grains. The proportion of outlier SNPs associating with phenotypic variation, however, largely depended on whether we considered a neutral structure with 5 genetic groups (73.7%) or 11 populations (13.5%), indicating that population stratification greatly affected our results. Finally, chromosomal inversions were enriched for both SNPs whose allele frequencies shifted along elevation as well as phenotypically-associated SNPs. Altogether, our results are consistent with the establishment of an altitudinal syndrome promoted by local selective forces in teosinte populations in spite of detectable gene flow. Because elevation mimics climate change through space, SNPs that we found underlying phenotypic variation at adaptive traits may be relevant for future maize breeding.

Fluctuation of ecological niches and geographic range shifts along chile pepper's domestication gradient.

Domestication is an ongoing well-described process. However, while many have studied the changes domestication causes in plant genetics, few have explored its impact on the portion of the geographic landscape in which the plants exist. Therefore, the goal of this study was to understand how the process of domestication changed the geographic space suitable for chile pepper (Capsicum annuum) in its center of origin (domestication). C. annuum is a major crop species globally whose center of domestication, Mexico, has been well-studied. It provides a unique opportunity to explore the degree to which ranges of different domestication classes diverged and how these ranges might be altered by climate change. To this end, we created ecological niche models for four domestication classes (wild, semiwild, landrace, modern cultivar) based on present climate and future climate scenarios for 2050, 2070, and 2090. Considering present environment, we found substantial overlap in the geographic niches of all the domestication classes. Yet, environmental and geographic aspects of the current ranges did vary among classes. Wild and commercial varieties could grow in desert conditions, while landraces could not. With projections into the future, habitat was lost asymmetrically, with wild, semiwild, and landraces at greater risk of territorial declines than modern cultivars. Further, we identified areas where future suitability overlap between landraces and wilds is expected to be lost. While range expansion is widely associated with domestication, we found little support of a constant niche expansion (either in environmental or geographical space) throughout the domestication gradient in chile peppers in Mexico. Instead, particular domestication transitions resulted in loss, followed by capturing or recapturing environmental or geographic space. The differences in environmental characterization among domestication gradient classes and their future potential range shifts increase the need for conservation efforts to preserve landraces and semiwild genotypes.

Superheroes and masterminds of plant domestication.

Domestication is one of the most fundamental changes in the evolution of human societies. The geographical origins of domesticated plants are inferred from archaeology, ecology and genetic data. Scenarios vary among species and include single, diffuse or multiple independent domestications. Cultivated plants present a panel of traits, the "domestication syndrome" that distinguish them from their wild relatives. It encompasses yield-, food usage-, and cultivation-related traits. Most genes underlying those traits are "masterminds" affecting the regulation of gene networks. Phenotypic convergence of domestication traits across species or within species between independently domesticated forms rarely coincides with convergence at the gene level. We review here current data/models that propose a protracted transition model for domestication and investigate the impact of mating system, life cycle and gene flow on the pace of domestication. Finally, we discuss the cost of domestication, pointing to the importance of characterizing adaptive functional variation in wild resources.