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However, because there has been considerable change in the areas covered by these habitat types over the last years Kraft et al.
In contrast, the pungency of wild chile pepper fruit repels small mammals that function as seed predators, but directs their dispersal to safe sites under nurse trees where germination, recruitment and establishment have higher probabilities Tewksbury and Nabhan, ; Carlo and Tewksbury, Thus, the directed dispersal adaptations of wild chile peppers afforded to them by the pungency of their specialized SMs—their capsaicinoids—have conferred to them a level of reproductive fitness that has incidentally allowed them to be present in abundance and accessible to human foragers in the Neotropics for millennia.
Changes in Secondary Metabolite Intensity With Chile Domestication What are the traits that have been modified as a result of selection under cultivation that have made modern and fully domesticated varieties of chile peppers so poorly adapted to the natural Neotropical habitats? The complexity and specificity of SMs as chemical mediators of biotic interactions of both wild and domesticated C. Ecological and cultural interactions shaping diversity of chile peppers Capsicum annuum L.
A Graphic illustration of SMs as chemical mediators of ecological interactions with wild C. Illustration designed by Frida Isabel Luna-Vallejo. B Map of Mexico showing indigenous territories, contrasted by colors.
The symbols identify particular ecological zones where certain indigenous groups have persisted in modern times. All indigenous groups represented here have documented uses of chile peppers. C A representative sample of the wider array current morpho-typic diversity and levels of domestication of chile peppers across Mexico.
Wild populations of chile pepper have coexisted and coevolved with many different organisms of tropical origin. Figure 1A focuses on two types of biotic interactions with wild Capsicum species: mutualistic and antagonistic.
Every particular plant interaction is regulated by some SM produced and expressed in a particular organ, at a certain phenological stage, in response to specific biotic or abiotic signals. Chile pepper interactions have been strongly influenced by humans and cultural diversity in Mesoamerica over the last 10, years.
The cultural diversity present in modern Mexico, and a sample of the wide morphological variation and levels of domestication that are currently found in Mexican chile peppers are shown in Figures 1B,C. The variation in Mexican chile peppers also applies to the chemical compounds, which may help explain the wide differences in fruit taste and flavor for different purposes and uses across Mexico.
Chen et al. Studies that have compared chemical defense traits in wild crop relatives and their cultivated counterparts are increasing in number, and their outcomes consistently show that domesticated plants provide a better food resource for herbivores than their more toxic wild progenitors.
Several studies provide evidence of such changes in the chemical ecology and biotic interactions along a domestication gradient Holt and Birch, ; Benrey et al. These widely-observed trends seem to contextualize, if not explain, shifts in the chemical defenses of C. To date, most studies of SMs in C. In addition, there are few ecological field studies of how capsaicinoids in wild Capsicum species of arid North America and tropical South America mediate relationships with native fauna, but they do not specify which capsaicinoid s drive those interactions Tewksbury and Nabhan, ; Tewksbury et al.
Most analyses have concentrated on capsaicinoids and few have included other SMs, such as phenolics and carotenoids. The presence of SMs in different organs and genotypic backgrounds may help explain the existence of natural sources of genetic resistance in Capsicum to particular herbivorous pests and seed predators.
The identities of most SMs remains incomplete among wild C. However, genetic resistance to Huasteco pepper virus has been documented for wild C. Of the known cases of genetic resistance among domesticated chile peppers are their tolerance to Phytophthora capsici and root knot nematodes, first documented in the Criollo de Morelos landrace—CM Pegard et al.
Crop domestication can lead to a decrease in SMs associated with pest resistance, a trend corroborated by Meyer et al. However, other SMs, such as capsaicinoids, have dramatically increased within some natural and domesticated chile pepper landraces e.
Balancing selection operated in ways that transformed some wild polymorphic populations into fully-domesticated but still heterogeneous C. We place particular emphasis on levels of SMs and other adaptations that appear to confer reproductive fitness to Capsicum populations in Neotropical habitats. Other Changes Occurring With Domestication of Chile Peppers We do not wish to presume that shifts in SMs were the only changes which have occurred with the domestication of Capsicum species in Neotropical habitats.
We wish to briefly mention several other traits of adaptive significance in Neotropical habitats.
Loss of Dispersal Mechanisms Wild chile peppers are naturally dispersed by frugivorous birds to the understory of selected nurse plants Tewksbury and Nabhan, ; Carlo and Tewksbury, , while domesticated chiles depend on human intervention for dispersal. Seed dispersal often involves lost of an abscission zone from some part of the plant. Fruits of wild chile peppers separate easily from the receptacle at maturity.
Fruits of domesticated peppers remain firmly attached to the plant. Mature wild chile pepper fruits are consumed and effectively dispersed by a variety of frugivorous Neotropical birds. Domesticated peppers are either too large, or are not attractive to nor dispersed by most Neotropical birds.
Different SMs may mediate seed dispersal in wild chiles, but carotenoids in the fruit pulp probably are likely the most important due to bird attraction by their red color. The pyrazine fragrances of chile peppers may also serve to attract certain birds. Loss of Seed Dormancy Most wild chile pepper seeds have staggered seed dormancy, which allows germination and recruitment when optimal conditions occur in a more variable and uncertain environment.
Domesticated chiles do not exhibit any seed dormancy Pickersgill, Therefore, domesticated chiles would likely have poor recruitment, survival and fitness if placed in most naturally wild environments.
Seed dormancy in most wild Capsicum species is mediated by SMs such as ABA, a plant regulator that inhibits seed germination Marrush et al. Wild chile pepper seeds with thick lignified testas become increasingly impermeable to water on drying.
This feature is disadvantageous for—if not absent from—most domesticated crop seeds, not only because these seeds germinate slowly, but also because they may require prolonged soaking to remove inhibitors from the seed coat Randle and Honma, ; Pickersgill, ; Carlo and Tewksbury, Therefore, domesticated chile peppers generally have thinner testae than their wild progenitors. Changes in Organ Size and Quantity As part of the domestication syndrome, changes in secondary metabolite content may be correlated with other physical and chemical traits, such as nutrient content, size, or biomass Chen et al.
Compared to most domesticated landraces, wild Capsicum species exhibit smaller leaves, flowers, fruits and seeds, but a larger number of these organs per plant Pickersgill, These characteristics—such small but numerous leaves and seeds—confer adaptability, stress reduction, survivability, and bet-hedging strategies to wild chile peppers for the production and dispersal of their seeds in Neotropical habitats Tewksbury et al.
Increased Morphological Variation According to Chen et al. This factor also is especially marked in the parts of the chile pepper plant used by Mesoamerican cultures. While domesticated chile peppers vary greatly in fruit size and shape, and to a lesser extent in color, wild C. In certain coastal Neotropical habitats, chile pepper fruits are selected for particular colors and shapes, said to be the best for seasoning turtle meat, while others, of different color and shape, are known as perfume peppers because they have a fragrant aroma as well as pungency.
All SMs in Capsicum species, including carotenoids, flavonoids, capsaicinoids, and ascorbic acid, are to some extent, linked with these morphological traits. Boster has deftly summarized the many references documenting the pronounced differences in morphology between wild and domesticated peppers.
Changes in Plant Habit Related to Resource Partitioning Selection for increased harvest index ratio of harvested to total biomass produced per plant may result in reduced or suppressed lateral branching Pickersgill, Reduced number of inflorescences per plant and producing more synchronous fruit ripening on an individual plant and within a stand, facilitating harvesting of the stand as a whole. Fewer nodes and shorter internodes, greater synchronization of maturation of vegetative branches and fruit ripening is also favored by a determinate habit.
Changes in Reproduction In Capsicum species, floral phenology and pollination, as well as fruit and seed development are influenced by different SMs. For example, carotenoid and flavonoid derivatives are secondary metabolites in the flower that attract pollinators. Similarly, fruit and seed dispersal are mediated by SMs which serve to attract seed dispersers. Simultaneously, fruit and seed protection is mediated by particular SMs capsaicinoids and phenolics that repel predators of fruits and seeds.
Wild C. Flower initiation is late, but once initiated is persistent and very prolific, with overlapping stages of flower and fruit development over the season. Fully domesticated C. Most of the fully domesticated chile pepper land races exhibit determinate growth under cultivation, with more rapid onset of flower initiation, fruit development and ripening. For such reasons, fruit and seed production of fully domesticated chile landraces would be almost impossible under natural wild environments in the Neotropics.
Loss of Chemical or Physical Protection Against Biotic and Abiotic Stresses Many other domesticated crops have partially or completely lost the SMs that protect their wild relatives against predators herbivores, plant pests and pathogens , and abiotic stresses drought, salinity, heat, frost, daming radiation, etc.
However, this trend does not necessarily hold true for most domesticated C. Capsaicinoids and other SMs are synthesized in the placental tissue of domesticated chile fruits after flowering as part of fruit development.
In other words, in domesticated chiles, SMs may play a small role in chemical defense of plant tissues before fruit and seed development Meyer et al. Protection of wild chile pepper fruits in populations against predators is mostly conferred by capsaicinoids, although flavonoids and phenolics may also play protective roles against predators.
Where they lack nurse plant protection in Mesomerican milpas, domesticated chile peppers must rely on farmers themselves to evict or to reduce the damage potentially wreaked by mammalian predators and browsers Pickersgill, ; Gepts, ; Padilha and Barbieri, With regard to protection against abiotic stresses, wild chile pepper plants employ SMs such as flavonoids, phenolics and vitamin C for protection against drought, heat and daming radiation.
In particular, carotenoid derivatives confer protection against plant cell oxidative reactions caused by lethal radiation, such as direct sunlight and UV light Wahyuni et al.
The hottest chile peppers belong to C.
Domesticated landraces of C. Agroecological Context of Milpa Cultivation as a Selective Pressure Lack of both seed dormancy and a facultatively perennial plant habit probably enabled the shift from avian dispersal of fruits under nurse plant canopies in the wild to open cultivation of annual plants with non-dormant seeds in milpa agro-ecosystems. The loss of ecological interactions with birds and nurse plants due to intentional seed-saving and dispersal by humans must have generated incidental changes in SMs.
Shifting the patterns of SMs through such selection could explain, in part, the emergence of new chemotypes, genotypes and morphotype landraces under cultivation in milpas within the Neotropics.
The Mesoamerican milpa agroecosystem may have gradually replaced the nurse plants in agroforestry systems during the early domestication of C. Curiously, this is roughly the time period when a new meme —a chile-processing technology and associated culinary techniques—first became evident in the prehistoric cultures of south-central Mexico.
This technology was called mollicaxtli in Nahuatl now molcajete today in Spanish, and consists of a round three-legged, grinding bowl and pestle for crushing dried spices, made out of fired clay or volcanic stone Vela, The molcajete's sudden emergence and wide diffusion suggests that domesticated chile pepper were not merely being eaten fresh, but surplus harvests were being dried and stored between growing seasons for use as a dried spice, condiment, medicine or vermifuge.
Thus, a new technology molcajetes and its associated culinary uses, as well as seed saving and trade beyond their ancestral habitats may have accelerated selection for a wider range of Neotropical habitats and overall diversification of domesticated chile pepper landraces. There is limited evidence that the mixes of capsaicinoids found in cultivated chile varieties are also more variable than those in wild populations, but comparable sampling has been poor. Neverthless, we see evidence for both H2 —a diversification of the levels of potency—and H3 —an intensification of potency of selected SMs with chile pepper domestication.
In the case of milder less pungent chile peppers, we assume that farmers' protection of the plants compensates to some extent for lower levels of chemical defenses.
Haak et al. While capsaicinoids remain the most important plant chemical defenses in most domesticated chiles as they are in wild peppers, the roles of other secondary metabolites found in lower concentrations should not be dismissed.
Brown et al. Nevertheless, several lines of research agree that the origin of the domesticated C. In other words, the precise location or locations of domestication of C.