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

Abstract

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.

Capturing the distribution as it shifts: chile pepper (Capsicum annuumL.) domestication gradient meets geography

“…Many crops have been reported to evolve adaptations to new climates through wild to landrace introgression (reviewed in (Janzen et al, 2019)), a process that may be hampered if a crop population’s geographical overlap is strongly diminished (Zhang et al, 2014). In chile pepper, cultivated and wild forms of C. annuum can easily hybridize (Eshbaugh, 2012; Pérez-Martínez et al, 2022). Often wild chile peppers establish in milpas and backyards, providing opportunities for wild to landrace gene flow (Guzmán et al, 2005; González-Jara et al, 2011; Pérez-Martínez et al, 2022).…”

“…In chile pepper, cultivated and wild forms of C. annuum can easily hybridize (Eshbaugh, 2012; Pérez-Martínez et al, 2022). Often wild chile peppers establish in milpas and backyards, providing opportunities for wild to landrace gene flow (Guzmán et al, 2005; González-Jara et al, 2011; Pérez-Martínez et al, 2022). Small-holder plots that steward this evolutionary process in situ should be encouraged in regions where wild and landrace distributions overlap.…”

“…glabriusculum , mainly) were characterized as plants morphologically corresponding to C. annuum var. glabriusculum (perennial plants with small erect fruits, small flowers) that may occur in human-managed spaces such as back-yards, small family plots or milpa agroecosystems, where they grow spontaneously as arvenses (from latin word arvum: ploughed; i.e associated to ploughed land) and are tolerated/consumed yet retain a wild-like phenotype (Aguilar-Meléndez et al, 2009; Pérez-Martínez et al, 2022). Landraces ( C. annuum var annuum , mainly) are identified as such by farmers and communities and are typically grown through traditional agriculture with a tendency to pertain to particular cultural regions in association to specific uses by local communities.…”

Population structure in diverse pepper (Capsicum spp.) accessions

“…L.), four levels of domestication are typically identified: wild, semi-wild, landrace, and commercial peppers [ 5 ]. Nevertheless, while genome wide levels of diversity are higher amongst landraces than commercial peppers, there can be stronger (e.g., Chile de Agua) or weaker (e.g., Mirasol) fixation for all the classic domestication syndrome traits within specific lineages of landraces and the degree to which they hybridize with wild peppers also varies [ 6 ].…”

Non-random distribution of maax pepper plants (Capsicum annum var. glabriusculum) in Mayan homegardens: Effects on plant size, fruit yield and viral diseases

“…southeastern Mexico) where it co-occurs with its domesticated relatives (Capsicum annum var. annuun) (Latournerie et al, 2001;Aguilar-Meléndez et al 2009;Pérez-Martínez et al 2021). In natural habitats, wild pepper relies heavily on birds, which deposit viable seeds beneath the canopy of woody perennials, particularly those that produce eshy fruits and offer birds suitable perches and food (Tewksbury et al 1999;Carlo and Tewksbury 2014).…”