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2The University of Reading, Department of Agricultural Botany, School of Plant Sciences, Whiteknights, P.O. Box 221, Reading RG6 6AS, UK; 3Jardín Botánico, Instituto de Biología, Universidad Nacional Autónoma de México, Apartado Postal 70-614, México, D.F. 04510, México; 4Instituto de Ecología, Universidad Nacional Autónoma de México, Apartado Postal 70-275, México, D.F. 04510, México; and 5Instituto de Biología, Universidad Nacional Autónoma de México, Apartado Postal 70-614, México, D.F. 04510, México
Received for publication January 6, 1998. Accepted for publication August 20, 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Cactaceae • columnar cacti • domestication • Mixteca • morphological variation • Stenocereus stellatus • Tehuacán Valley
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, 1868
; Schwanitz, 1966
; Harlan, 1992
). Such divergence is a result of artificial selection and other evolutionary forces determined by manipulation of plants and animals by humans. In plants, the process of domestication has been generally associated with cultivation in controlled environments out of their wild populations (Harlan, 1992
; Zohary and Hopf, 1993
). Although humans have also practiced different forms of manipulation of wild populations (Rindos, 1984
; Harris, 1989
; Casas et al., 1997a
), the role of these forms of plant manipulation in domestication has not been evaluated.
Different forms of management of wild populations in situ have been reported in a number of plant species in Mexico (Alcorn, 1981
; Bye, 1993
; Caballero, 1994
; Casas and Caballero, 1996
; Casas et al., 1996
), and they seem to be common ways of plant manipulation by people in Mesoamerica (Casas et al., 1997a
). Casas and Caballero (1996)
have suggested that domestication under forms of management in situ (in situ domestication) may be an attractive model for explaining domestication of some plant species, especially long-lived perennials. However, the demonstration and evaluation of this process are yet to be done.
In this study, the case of Stenocereus stellatus (Pfeiffer) Riccobono is analyzed. This is a columnar cactus species endemic to central Mexico, occurring in the wild as part of tropical deciduous and thorn-scrub forests. It is also cultivated in home gardens, and some wild populations are managed in situ since it is a useful species (Casas et al., 1997b
). This situation offers the possibility of studying the evolution of this species under domestication processes and determining whether domestication has been significant under forms of management of wild populations in situ.
During August and September, the season when fruits of S. stellatus are ripe, it is possible to observe a significant morphological variation in fruit characteristics. This variation might be phenotypic expression influenced by natural environmental conditions since the range of S. stellatus covers altitudes from 600 to 2000 m, levels of precipitation between 300 and 800 mm/yr, annual mean temperatures from 17° to 24°C, and soils derived from limestones, sandstones, volcanic rocks or alluvial deposits. Conversely, this morphological variation may have a genetic basis and be favored by the self-incompatible sexual reproduction system, which, along with vegetative propagation, is characteristic of this species (Casas, 1997
).
Nevertheless, the variation in fruits could be also the result of manipulation of this species by humans. According to archaeological information obtained in caves from the Tehuacán Valley, S. stellatus has apparently been used by people for more than 5000 yr (MacNeish, 1967
; Smith, 1967
); Currently, ten different indigenous groups inhabiting the area use and manage this species mainly because of its edible fruits. Casas et al. (1997b)
reported that management of wild populations of S. stellatus in situ is carried out by sparing some desirable phenotypes, while removing others during clearance of vegetation and sometimes enhancing numbers of the spared desirable phenotypes by planting their branches. Cultivation of this species is practiced mainly in home gardens, where desirable phenotypes are vegetatively propagated and new variation is incorporated through tolerance of volunteer seedlings.
Pulp color, flavor, amount of edible matter, peel thickness, and spininess of the fruits are the most significant characteristics used by people in folk classification of variants, in assessing quality of products, and in selecting individuals of S. stellatus for preferential propagation (Casas et al., 1997b
). Manipulation of this plant species by people thus appears to involve artificial selection. This seems to be particularly intense in home gardens, where manipulation of S. stellatus is by planting and replacing individuals continually. However, it could also be significant in managed in situ populations, where selection is mainly directed to increase frequencies of good phenotypes existing in wild populations (Casas et al., 1997b
).
The main hypothesis of this study was that if artificial selection has been significant, both management in situ and cultivation of this species might have changed to some extent patterns of morphological variation (especially in those characters that are direct targets of human selection) from those occurring in wild and unmanaged populations. Accordingly, the purpose of this study was to analyze patterns of morphological variation in wild, managed in situ, and cultivated populations of S. stellatus, in order to examine whether human selection has modified the phenotypic structure of manipulated populations. This study also focused on comparing morphology of individuals from two regions (the Tehuacán Valley and La Mixteca Baja), in order to examine to what extent patterns of morphological variation in populations can be related to environmental factors.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). La Mixteca Baja includes the northwest of Oaxaca, the southeast of Puebla, and the northeast of Guerrero states. It is a mountainous region with altitudes ranging from 600 to 3000 m. Vegetation varies from thorn-scrub and tropical deciduous forests in the lower dry and warm settings to pine forests in the higher wet and temperate areas.
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Home gardens were the sampling units in cultivated populations. Nearly 10% of the home gardens in a village were sampled at random. A number was given to each home garden in a village, and then a list of numbers was drawn from a table of random numbers. With a similar method, 10% of the total number of individuals within the home gardens selected were randomly sampled.
Due to the natural clonal propagation of S. stellatus, it was difficult to identify isolated individuals in the field. For purposes of sampling, an individual was considered in this study as a unit of branches emerging together from the ground. Because morphological comparisons included reproductive parts, only individuals at reproductive stage were sampled.
A total of 324 individuals were sampled, 89 of them from the wild populations, 90 from the populations managed in situ, and 145 from home gardens (Table 1).
Morphological characters analyzed
A total of 23 characters were analyzed (Table 2). According to ethnobotanical information (Casas et al., 1997b
), characters such as pulp color and flavor, spininess and thickness of the peel, and amount of edible matter were considered to be direct targets of human selection. Other characteristics, which, according to local people, are not targets of selection, were also included in order to have a reference of general patterns of morphological variation independent of human influence. These included characters used by botanists for the taxonomy of columnar cacti (Bravo-Hollis, 1978
; Gibson and Horak, 1978
).
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). Alternative variants of each qualitative character were considered as discrete character states. For the remaining quantitative characters, three to five measurements for each character per individual were obtained to calculate a representative mean value. Length and diameter of the highest branch of each individual sampled were measured by a measuring stick and a forestaff, respectively. Number of stem ribs was counted always at the middle part of the branches selected. Width and depth of stem ribs were measured by a caliper, also at the middle part of the branches selected. Number of spines per areole, longitudinal distance between areoles, and size of the central spine in areoles (estimated as the product of the maximum length of the spine and the diameter in the middle part of the spine) were recorded in randomly selected areoles.
Fruit size was estimated by measuring maximum diameter and length of fruits and then calculating the volume as the volume of oblate spheroids by the formula v = (4/3)
a2b, where a is half the transverse diameter of the fruit and b is half its length.
The total number of areoles per fruit was counted. The number of areoles per square centimeter was measured by using a card with 2-cm2 holes always situated on the equatorial plane of the fruits. All complete or incomplete areoles included in the squared holes were counted and then divided by 2 to have a measure per square centimetre. Thickness of the peel was measured with a caliper always in the equatorial plane of the fruits.
Percentage of edible part of the fruit (pulp and seeds) was calculated as the ratio of the mass between the pulp and seeds and the total mass of the fruit, including the peel. The percent water of pulp mass was estimated as the ratio: (dry pulp mass/fresh pulp mass) x 100.
Total number of seeds per fruit was counted and their total mass measured. Mean seed mass was estimated by weighing a sample of 100 seeds per fruit and dividing by 100 to obtain the average seed mass. Percent of seed to pulp was estimated from the ratio of the total mass of seeds to the total mass of the edible portion per fruit.
Methods of data analysis
Patterns of morphological similarity/difference were analyzed by multivariate statistical methods, as in other studies such as Pickersgill, Heisser, and McNeill (1979)
, Casas and Caballero (1996)
, Colunga-García Marín, Estrada-Loera, and May-Pat (1996)
, and Mapes et al. (1996)
.
Principal Component (PCA) and Discriminant Function Analyses (DFA) were directed to analyze patterns of individuals within each region in order to visualize possible differences among populations according to their way of management. DFA was also aimed at evaluating the overlap between wild, managed in situ, and cultivated populations in their overall morphology, by looking at misassignment of individuals from their original groups. Evaluation of the discriminant functions derived from DFAs by one-way MANOVAs was directed to test the null hypothesis that there are no significant differences between wild, managed in situ, and cultivated populations. The eigenvectors resulting from PCAs and the standardized discriminant function coefficients resulting from DFAs were used to identify the characteristics that most significantly contribute to classifying individuals (Sneath and Sokal, 1973
; Krzanowski, 1990
). Cluster Analysis (CA) was performed to examine the morphological similarity, at population level, between the populations studied of the two regions analyzed together. The purpose was to visualize possible differences between populations of the Tehuacán Valley and La Mixteca, which would be possibly related to the environmental differences existing among these regions. CA was also directed to visualize the morphological similarity/difference of populations under a similar management across the regions.
Basic data matrices were constructed with morphological characters considered as variables. PCAs were performed with the mean values per individual of each of the 19 quantitative characters and the character states of the qualitative characters. DFAs included only quantitative characters. CA included the mean values of the quantitative characters per population and the proportion of individuals per population producing fruits with spherical form, red peel, red pulp and sweet flavor. The individual plants from each region analyzed by PCAs and DFAs, as well as the 19 populations, in CA were considered as Operational Taxonomic Units (OTUs). Numerical values of characters of the basic data matrices were standardized by subtracting the mean value of the character per individual or population from the average for this character over all individuals or populations studied, and then dividing by the standard deviation for this character in the sample of individuals or populations.
PCAs were performed on correlation matrices between characters calculated by using the Pearson correlation coefficient (Sneath and Sokal, 1973
). For DFAs, the individuals were arranged in three groups according to form of management (wild, managed in situ, and cultivated). One-way MANOVAs for evaluating population differences were performed using Wilks' Lambda as the test statistic. CA was performed by calculating a similarity matrix between populations using the Euclidean Distance coefficient and then processing this matrix by the UPGMA method (Sneath and Sokal, 1973
). CA and PCAs were carried out using NTSYS-PC version 1.8 (Rohlf, 1993
), while DFAs were performed by SYSTAT version 7.0 (SYSTAT, 1997
).
Two-way analyses of variance tested statistical significance of differences for each quantitative morphological character among populations according to their region of provenance (Tehuacán and La Mixteca), and according to their management regime (wild, management in situ, and cultivation). Tukey's highest significant difference tests (HSD, 95%) were performed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Interactions between region and type of management were significant in branch diameter, rib dimensions, spine size, and percent water of pulp, which were significantly different only among populations of the Tehuacán Valley, as well as in number and density of areoles in fruit, and seed mass, which presented more pronounced differences among populations of the Tehuacán Valley.
The highest correlations between characters were those between peel thickness and percent of pulp in fruits (r = -0.81 in Tehuacán and r = 0.72 in La Mixteca), as well as between fruit size and density of spines in peel (r = -0.77 in Tehuacán and r = -0.60 in La Mixteca), fruit size and total seed mass (r = 0.75 in Tehuacán and r = 0.69 in La Mixteca).
In all the populations of Tehuacán, the proportion of individuals producing spherical fruits was higher than that producing the elongated ones (Table 7), whereas in La Mixteca, nearly one-half of the individuals sampled produced fruits of each form. Most of the individuals of the two regions produced fruits with red peel and pulp, but >40% of the cultivated individuals from La Mixteca produced fruits with green peel and pulp colors other than red. Most of the wild individuals produced sour fruits, whereas most individuals from the managed in situ and cultivated populations produced sweet fruits. However, the proportion of individuals producing sweet fruits was generally higher in La Mixteca than in Tehuacán.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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and Casas et al. (1997b)
that human management has significantly influenced morphological divergence of both managed in situ, and cultivated populations from wild populations of this species and that, therefore, domestication may be caused not only through cultivation but also through management of wild populations in situ. Casas and Caballero (1996)
and Casas et al. (1997a)
suggest that in situ domestication may be a model by which to investigate domestication in perennial plants, especially those with outbreeding reproductive systems, because of the difficulties for fixation of desirable characters by direct sowing of seeds from desirable phenotypes. The case of S. stellatus, therefore, appears to be an example for developing such a model. The overlaps between the different types of populations, identified by both PCAs and DFAs (Figs. 2, 3; Table 4) reveal important information for analyzing the process of domestication of S. stellatus. These overlaps are explicable because, according to local people, the introduction of individuals from wild and managed in situ populations to home gardens is continually being carried out. These overlaps indicate that commonly cultivated phenotypes occur also in wild and, especially, in managed in situ populations, although in low frequencies, and that wild phenotypes have maintained their morphological characteristics in managed in situ populations and when they are brought to cultivation in home gardens. This observation, along with the fact that these characteristics are expressed differently in individuals of different origin cultivated within a same home garden, suggests that such characteristics have an important genetic component. This would indicate then that changes in morphological characters may be inherited and that artificial selection on these characters is causing the morphological differences.
Overlaps between wild and managed in situ populations would be expected because managed in situ populations derived directly from wild populations. However, the overlaps are relatively small and these types of populations have diverged significantly, illustrating that artificial selection under management in situ has also been significant. Groups of managed in situ and cultivated individuals appear to be the most similar among themselves since overlaps between them were the most frequent. The information obtained thus indicates that morphological divergence is significant between wild and managed in situ populations but especially strong between wild and cultivated populations, probably because artificial selection is particularly intense under the continual planting and replacing of individuals cultivated in home gardens.
Although part of the phenotypes of managed in situ and cultivated populations originated from wild populations, some cultivated phenotypes were rare or not observed in the wild. This is particularly the case of individuals with large fruits and pulp colors other than red. Thus, only 2.3% of the individuals sampled in wild populations were found presenting pink and yellow pulp, whereas other pulp colors (purple, orange and white) were not observed in the wild. On the other hand, nearly 42% of individuals sampled in cultivated populations of La Mixteca were of these phenotypes. The questions are still open of whether these phenotypes originated in the wild and were carried to home gardens or if they originated in home gardens and escaped to the wild. But, regardless of these possible origins, it seems to be clear that success of such phenotypes is low in the wild and it only may be higher under human protection. In other words, domestication of S. stellatus appears to have been operating by protecting and enhancing individuals whose morphological characteristics are favorable to humans but that are scarce (some of them probably absent) in the wild.
The most important characters for explaining the patterns of variation in populations and the ordination of individuals in PCA and DFA are: (1) fruit size (larger among cultivated individuals); (2) density of spines in fruits (higher in fruits of wild individuals); (3) peel thickness (thicker in fruits of wild individuals); (4) total mass of seeds (higher in fruits of cultivated individuals); (5) mean seed mass (heavier in cultivated individuals); and (6) proportion of edible part in fruits (higher in cultivated individuals). Pulp color was relevant in the classification of groups only in La Mixteca, where individuals with "not red" pulp fruits were abundant in cultivated populations, whereas flavor of fruits was relevant in the Tehuacán Valley, where the proportion of individuals producing sweet fruits was markedly different between wild, managed in situ, and cultivated populations. Among the vegetative characters, only the dimensions of ribs and branches seemed relevant (larger dimensions in cultivated individuals).
Most of these characters are those that constitute direct targets of selection by people (Casas et al., 1997b
), which reinforces the conclusion that artificial selection is the crucial factor for explaining the divergence between wild and manipulated populations. The only exceptions are amount and mass of seeds, which were significant characters even though people informed us that they are not targets of selection. Changes in these characteristics might be a consequence of selection for larger fruits because, since the pulp is formed by funiculus (Bravo-Hollis, 1978
), both the amount of pulp and fruit size would be related with amount and size of funiculus. In fact, correlation between these characters presented relatively high values. However, a possible occurrence of human selection on this character in the past should not be discarded since consumption of seeds separately from pulp apparently has occurred since prehistoric times (Callen, 1967
; Casas et al., 1997b
).
Morphological variation of S. stellatus appeared to be influenced also by environmental conditions. Thus, CA clustered populations in part according to the region from which they originated and univariate analyses of variance found significant differences between populations of the two regions in most of the morphological characteristics analyzed. The populations sampled in the two regions present differences in annual mean temperatures, soils, and vegetation types (Table 1). However, the most clear environmental difference between the regions, and probably the most significant for explaining morphological variation, is annual precipitation, which is significantly higher in la Mixteca (720.5–763.7 mm) than in the Tehuacán Valley (440.6–590.0 mm).
Some of the morphological characters distinguishing populations of S. stellatus across the regions appear to be affected by differences in rainfall. This is the case of the dimensions of branches, which are related with the turgidity of branch tissue. In general, branches of this species presented greater length and diameter in La Mixteca than in Tehuacán. Differences in robustness of the branches were pronounced among wild and managed in situ populations, which are exposed to natural environmental conditions, but not among cultivated populations, which are exposed to environments that occasionally are watered by people. Fruit size would also be expected to be influenced by availability of water, since the bigger fruits from La Mixteca generally presented a higher proportion of water in pulp than the smaller fruits from Tehuacán. However, the correlation between fruit size and proportion of water in pulp is low (0.56 in Tehuacán and 0.44 in La Mixteca), indicating that fruit size is not simply determined by amount of water.
Qualitative morphological characters were also different across the regions. Thus, a higher proportion of individuals in populations from La Mixteca produced fruits with green peel, pulp color different than red and sweet flavor (Table 7). But, apart of human selection, factors influencing such characteristics in wild populations are unknown.
In conclusion, although populations of S. stellatus of the two regions differ morphologically, probably due to environmental differences, within each region wild and manipulated populations have diverged morphologically presumably due to artificial selection. Although the strongest level of divergence from wild populations was found to occur in cultivated populations, it is also significant in wild populations managed in situ. This strongly suggests that domestication in situ is an ongoing process in this plant species.
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FOOTNOTES |
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6 Author for correspondence, current address: Departamento de Ecología de los Recursos Naturales, Instituto de Ecología, UNAM, Apdo. Postal 27-3 (Xangari) C.P. 58089 Morelia, Michoacán, México.
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