ARTICLE IN PRESS

Journal of Arid Environments 72 (2008) 1997– 2010

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Journal of Arid Environments

journal homepage: www.elsevier.com/locate/jaridenv

Population genetics and process of domestication of

Stenocereus pruinosus (Cactaceae) in the Tehuacán Valley, México
F. Parra, N. Pérez-Nasser, R. Lira, D. Pérez-Salicrup, A. Casas 
Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Apartado Postal 27-3 (Santa Marı́a de Guido), Morelia,
Michoacán 58190, México

a r t i c l e in fo abstract

Article history: Population genetics of wild, managed in situ and cultivated populations of Stenocereus
Received 20 October 2007 pruinosus coexisting in Central Mexico were studied. We hypothesized that artificial
Received in revised form selection decreases genetic diversity in managed populations and influences differ-
28 May 2008
entiation of populations depending on the amount of gene flow. Nine wild, managed in
Accepted 20 June 2008
Available online 31 July 2008
situ and cultivated populations (264 individual plants) were studied through isozyme
analysis (10 loci). Genetic variation of S. pruinosus is the highest reported in columnar
Keywords: cacti species (e.g. HT ¼ 0.592). Genetic variation in cultivated populations (Ho ¼ 0.611,
Columnar cacti He ¼ 0.588) was slightly higher than in wild (Ho ¼ 0.556, He ¼ 0.583) and managed in
In situ conservation
situ populations (Ho ¼ 0.536, He ¼ 0.578), but differences were not significant. Most of
In situ domestication
the genetic variation occurred within populations, with low differentiation and high
Mesoamerica
Silviculture gene flow among all populations (FST ¼ 0.064, NmFST ¼ 3.659 and NmGST ¼ 3.803 in
Traditional agriculture average) associated to bat pollination, seed dispersal by birds and transportation of
vegetative propagules by people. Genetic distances were not correlated with geographic
distances and in most cases are lower between similarly managed populations.
Managed in situ and cultivated populations are important reservoirs of genetic diversity
of this species to be considered in conservation programs.
& 2008 Elsevier Ltd. All rights reserved.

1. Introduction

Domestication is an evolutionary process of plants and animals guided by humans mainly through artificial selection
(Darwin, 1859). It is a continuous process, which derives in morphological, physiological, behavioral, and genetic
divergences between populations of managed organisms and their wild relatives (Casas et al., 2007). The cultural area
known as Mesoamerica, comprising the territory from southern Mexico to northern Costa Rica is one of the main centers of
domestication of plants in the World (Harlan, 1975; Hawkes, 1983; Vavilov, 1951). In Mesoamerica, it is possible to study
the ongoing processes of artificial selection of plant species currently under domestication (Casas et al., 2007). For some of
these species, wild, semidomesticated, and domesticated populations coexist with continuous genetic interactions, thus
influencing the evolution of both crops and wild relatives. Therefore, this region is particularly interesting for studying
the natural and cultural factors influencing domestication. Ethnobotanical and evolutionary studies in Mesoamerica
have documented a broad spectrum of incipient processes of domestication that are particularly interesting, as they allow
the study of early phases of domestication which could in turn unveil how agriculture originated (Casas et al., 2007;

 Corresponding author.
E-mail address: acasas@oikos.unam.mx (A. Casas).

0140-1963/$ - see front matter & 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jaridenv.2008.06.007
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1998 F. Parra et al. / Journal of Arid Environments 72 (2008) 1997–2010

Colunga-Garcı́aMarı́n and Zizumbo-Villarreal, 2007; Colunga-Garcı́aMarı́n et al., 1986, 1996; Hughes et al., 2007; Zárate
et al., 2005). In this study, we analyze the genetics of wild and managed populations of the columnar cactus Stenocereus
pruinosus, a species of high cultural value under incipient process of domestication.
Columnar cacti have been used by peoples since the earliest phases of human occupation of the arid and semiarid
portions of Mesoamerica (Flannery, 1986; MacNeish, 1967). The highest diversity of these plants occurs in Mexico
(nearly 75 species), particularly in the Balsas river basin and the Tehuacán Valley in Central Mexico where 43 species have
been recorded (Valiente-Banuet et al., 1996). In these regions, columnar cacti are used as food, building material, fodder,
living fences, and fuel (Casas et al., 1999a). Some of these uses date back to nearly 10,000 years (MacNeish, 1967). Useful
products of all of these species are gathered mainly in the wild, but for 22 species of columnar cacti managed individuals
with favorable phenotypes to humans are let standing or intentionally propagated in areas where vegetation is cleared.
Twelve of these species are also cultivated in home gardens (Casas et al., 1999a). Therefore, these are also important areas
of domestication of columnar cacti.
According to Arias et al. (1997), S. pruinosus is an arborescent cactus up to 8 m in height. Branches are green with
pruinosus apexes and 5–8 ribs. Flowers are infundibuliform 7–10 cm in length growing in the branch apexes, with green
brownish external tepals and white internal tepals. Cortés-Dı́az (1996) reported that flowers have nocturnal anthesis with
self-incompatible breeding system being pollinated by bats. The ellipsoid fruits locally called ‘‘pitayas de mayo’’ may have
white, yellow, purple, orange and more commonly red pulp with black seeds. Vegetative propagation is common in both
natural and artificial environments, and individual plants derived from branches approximately 1.2 m in length produce
flowers 2 or 3 years after being planted (Casas et al., 1999a). This species is widely distributed in sem-iarid areas of the
states of Oaxaca, Puebla, Chiapas, Tamaulipas, Veracruz, and Yucatán (Bravo-Hollis, 1978).
S. pruinosus (Otto) Buxb. is one of the cactus species more intensely managed in Central Mexico (Casas et al., 1999a;
González-Insuasti and Caballero, 2007), as its fruits have the highest economic value of all columnar cacti species of that
region (Casas et al., 1999a). Fruits of this species are gathered in wild populations. There are also silvicultural managed in
situ populations constituted by individuals that were left standing, and sometimes propagated when forests were cleared
for establishing corn fields. This type of management commonly involves selection favoring individual plants with larger
and sweeter fruits, peel with lower density of spines, and pulp with various colors. Finally, in the semiarid Central Mexico
there are also cultivated populations of S. pruinosus, derived from plantations of branches from wild or in situ managed
individuals with desirable phenotypes according to the attributes mentioned above. Cultivated populations are established
mainly in home gardens. Thus, S. pruinosus can be considered as a plant under incipient domestication, with individuals
belonging to three categories of management: wild, managed in situ, and cultivated populations.
Artificial selection has caused significant divergence in these morphological characters between wild and managed
populations as it has been documented for species of columnar cacti (Arellano and Casas, 2003; Carmona and Casas, 2005;
Casas et al., 1999b; Cruz and Casas, 2002). Also, effects of artificial selection on population genetics of columnar cacti have
been documented in Polaskia chichipe (Gosselin) Backeberg (Otero-Arnaiz et al., 2005a, b), Escontria chiotilla (F.A.C. Weber)
Rose (Tinoco et al., 2005), Stenocereus stellatus (Pfeiffer) Riccob. (Casas et al., 2006), and Polaskia chende (Gosselin)
Backeberg (Ruı́z-Durán, 2007). These studies have generally found that managed in situ and cultivated populations have
slightly lower genetic variation than wild populations, but in the case of S. stellatus both managed in situ and cultivated
populations have more genetic diversity than wild populations. This last pattern appears to be due to traditional
management involving a continual replacement of individual plants within the plantations and the introduction of plants
from other areas. Population genetics studies have also documented high gene flow occurring among all populations
and therefore low genetic differentiation and structure of populations (Casas et al., 2007). In the case of Stenocereus
species, gene flow is greatly determined by pollinators, mainly the bats Leptonycteris curasoae and Choeronycteris mexicana
(Casas et al., 1999c), as well as several bird and bat species acting as seed dispersers.
According to Hawkes (1983) and Doebley (1992), domestication generally determines a decrease of genetic diversity in
managed populations of organisms compared with wild populations since domesticated stands commonly include a
selected fraction of the diversity existing in the wild. However, since the traditional management pattern has determined
high levels of genetic variation in S. stellatus, and S. pruinosus is more intensely managed than that species, in this study we
expected to find high levels of genetic diversity in managed in situ and cultivated populations. Also because of the
management intensity, we expected to find higher genetic differentiation between wild and managed populations than that
reported for S. stellatus, even when we expected to find high levels of gene flow because of the coexistence of populations in
distances within the range of movement of pollinators and seed dispersers. This study analyzes whether the traditional
management and incipient domestication of S. pruinosus has had consequences on the genetic diversity and structure of
wild, managed in situ and cultivated populations, and documents gene flow among these coexisting population types.

2. Methods

2.1. Study area

The study was conducted in the Tehuacán Valley, located at the southeast of the state of Puebla and the northeast of the
state of Oaxaca in Central Mexico (Appendix A electronic version only). It is a semiarid region with annual mean
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temperature of 21 1C, annual mean precipitation of 400 mm, and an extension of about 10,000 km2. The Tehuacán Valley is
conformed by a heterogeneous mosaic of environments with a total of 29 types of plant associations (Valiente-Banuet et al.,
2000) with columnar cacti forests being the most extended and varied vegetation types. S. pruinosus is a dominant element
in patches of vegetation covered with thorn-scrub and tropical deciduous forest established on alluvial soils.

2.2. Populations of S. pruinosus studied

The populations of S. pruinosus studied are located within the territories of the villages of San Luis Atolotitlán and
Coatepec, in the municipality of Caltepec, Puebla, and within the territories of the villages of San Rafael and Coxcatlán,
in the municipality of Coxcatlán, Puebla (Appendix A electronic version only).
Sampling sites were selected based on the different types of human management of this cactus species. We studied
three wild, three managed in situ, and three cultivated populations. Wild populations are located in the sites Santa Lucı́a
and Fiscal, within the territory of Coatepec, and in the site Cueva del maı́z, within the territory of San Rafael. All these
populations form part of patches of vegetation established on the bottom of alluvial valleys of ephemeral rivers, forming
part of tropical deciduous forest (Table 1). These wild habitats are relatively wetter than the surrounding vegetation, and
there the columnar cacti Pachycereus weberi (J. Coulter) Backeb., E. chiotilla, S. pruinosus, S. stellatus, and Pachycereus
hollianus (F.A.C. Weber) F. Buxb. are co-dominant with the trees Prosopis laevigata (Humb. et Bonpl. ex Willd.) M.C.
Johnston, Mimosa luisana Brandegee (Mimosaceae), Cytocarpa procera Kunth (Anacardiaceae), Gyrocarpus mocinnoi Espejo
(Hernandiaceae), Ceiba parvifolia Rose (Bombacaceae), Bursera morelensis Ramı́rez (Burseraceae), Ipomoea arborescens
G. Don (Convolvulaceae), and Parkinsonia praecox (Ruiz et Pavón) Harms (Caesalpinaceae).
The in situ managed populations are located in scattered areas used for seasonal agriculture of maize, near the villages
of San Luis Atolotitlán, Coatepec, and Coxcatlán which have been used for more than 100 years, with successive periods of
use and fallow. Cultivated populations are stands of individuals within home gardens and living fences of houses of local
farmers of the three villages studied (Table 1). The most distanced populations are the cultivated population from San Luis
Atolotitlán (C1) and the wild one from Coxcatlán (W3), separated by 31 Km, followed by populations from Coatepec and
San Luis Atolotitlán with respect to populations from Coxcatlán. The closest populations are the managed and cultivated
populations from San Luis Atolotitlán (Appendix B electronic version only).

2.3. Sampling of populations

A total of 30 reproductive individual plants per population were sampled. In wild populations, individual plants were
sampled in natural vegetation bordering the course of the ephemeral rivers. We followed transects collecting and geo-
referencing individual plants until completing the samples. Sampled area of wild populations averaged 2.2 ha. In the in situ
managed populations, where individual plants are more scattered, we collected all individual plants found until completing
the sample size in a sample area of 4 ha in average. In the case of cultivated populations, individual plants were sampled in
home gardens trying to equal sampled area of wild populations. Individual plants sampled were labeled to be identified in
further visits. Plant tissue for allozyme analysis was obtained from stem ribs of each individual plant sampled. Pieces of
nearly 15 cm3 of plant tissue per individual plant in each population were collected and frozen in liquid nitrogen (196 1C)
and then stored at 70 1C for conservation.

2.4. Allozyme analysis

Information on genetic variation of populations was obtained through standard methods for starch gel electrophoresis.
Enzymes extraction was conducted using the polyvinilpirrolidone phosphate extraction buffer developed by Mitton et al.

Table 1
Environmental aspects of the populations of Stenocereus pruinosus studied in the Tehuacán-Cuicatlán Valley

Population Location Elevation (m) Vegetation Rainfall (mm) Soils

Wild I Santa Lucı́a, Coatepec 1210 Tropical Deciduous Forest 544.4 Alluvial
Wild II Fiscal, Coatepec 1210 Tropical Deciduous Forest 544.4 Alluvial
Wild III ‘‘Cueva del Maı́z’’, Coxcatlán 1010 Tropical Deciduous Forest 394.6 Alluvial
Managed I San Luis Atolotitlán 1900 Seasonal maize fields 394.6 Derived from basaltic rocks
Managed II Santiago Coatepec 1853 Seasonal maize fields 394.6 Derived from basaltic rocks
Managed III Coxcatlán 1000 Seasonal maize fields 544.4 Regosols, calcalcareous
Cultivated I San Luis Atolotitlán 1903 Homegardens 394.6 Derived from basaltic rocks
Cultivated II Santiago Coatepec 1780 Homegardens 394.6 Derived from basaltic rocks
Cultivated III Coxcatlán 1145 Homegardens 544.4 Regosols, calcalcareous
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(1979). Plant tissue was ground in frozen mortars immersed in ice, adding about 300–330 ml of extraction buffer. Extract
was absorbed in filter paper wicks and stored in eppendorf tubes at 70 1C.
The enzyme analysis was done using two systems of electrode and gel buffers. The C buffer (Stuber et al., 1988) was used
to assay esterase (EST, Enzyme Commission number 3.1.1.1), glutamate oxaloacetate transaminase (GOT ¼ AAT, E. C. 2.6.1.1),
and acid phosphatase (ACPH, E. C. 3.1.3.2). The D buffer (Stuber et al., 1988) was used to assay malate dehydrogenase
(MDH, E.C. 1.1.1.37), menadione reductase (MNR, E.C. 1.6.99.2) and phosphoglucose isomerase (PGI, E.C. 5.3.1.9). Gels were
prepared using 12% starch (STARCHART) and 3% of sucrose. Horizontal electrophoresis was run at 60 mA for 5 h on the C
system, and 30 mA for 9 h on the D system. Interpretation of gels was conducted immediately after the optimum staining
was achieved. Stained gels were finally washed with water and fixed with 50% ethanol for 24 h.

2.5. Statistical analyses

Levels of genetic variation within and among populations of S. pruinosus were estimated from allelic frequencies
(Appendix C electronic version only), using the programs POPGENE version 1.21 (Yeh et al., 1997) and TFPGA version 1.3
(Miller, 1997). The number of alleles per locus (A), the percentage of polymorphic loci (P%), the observed heterozygosity
by direct counting (Ho), the expected heterozygosity (He(b)) (biased estimate) and the expected heterozygosity (He)
(unbiased estimate) (Nei, 1973) were calculated. Non-parametric Kruskal–Wallis H tests for significant differences in Ho,
He(b), and He were performed between wild, managed in situ and cultivated populations.
Fixation indexes or inbreeding coefficients were calculated by the formula F ¼ (HeHo)/He (Wright, 1951, 1978), in
order to estimate the excess of homozygotes in populations due to non-random mating. Significant differences between
observed and expected frequencies according to the Hardy–Weinberg equilibrium were estimated by X2 ¼ F2N(k1) with
[k(k1)]/2 degrees of freedom, where N is the sample size and k is the number of alleles per locus (Li and Horvitz, 1953).
Genetic diversity within and among populations of S. pruinosus was estimated at three levels: (1) total genetic diversity
(HT); (2) genetic diversity within populations (HS); and (3) genetic diversity between populations (DST). The proportion of
genetic diversity between populations GST was calculated for all populations and per management type. F-statistics
(Wright, 1951, 1978) were calculated to analyze the genetic structure of populations at three hierarchical levels: individuals,
subpopulations and total population. F-statistics were calculated for polymorphic loci using POPGENE 3.1. FIS and FIT are
correlations between pairs of alleles in one individual in relation to the subpopulation, and the whole population,
respectively. Both statistics allow identifying if a reduction in the number of heterozygote individual plants is occurring
because of non-random mating, in relation to the expected heterozygotes if mating was random, and if the population was
not subdivided, respectively (Luna, 1999). Negative values indicate excess of heterozygotes, whereas positive values
indicate excess of homozygotes. To determine whether FIS and FIT values were significantly different to zero, as expected in
Hardy–Weinberg equilibrium, a X2 test was performed using the formula X2 ¼ F2N(k1) with (k(k1))/2 degrees of
freedom, where N is the sample size and k the number of loci analyzed (Li and Horvitz, 1953). FST measures genetic
differentiation among populations obtained from the correlation between two alleles randomly chosen from each
population, and may have values between 0 (no differentiation) and 1. Significant differences of FST values observed with
respect the expected values in the equilibrium were tested by estimating X2 ¼ 2NFST(k1) with gl ¼ [(k1)(s1)] degrees
of freedom, where s is the number of subpopulations (Workman and Niswander, 1970).
Genetic distance between populations was estimated by Nei’s minimum genetic distances (Nei, 1972), and the
dendrogram was constructed through the UPGMA method. A Mantel test was used to assess the correlation between Nei’s
(1972) genetic distances and the geographical distances using TFPGA 1.3. Gene flow was calculated using NmGST and NmFST
parameters, assuming that there is gene flow when NmX1.

3. Results

3.1. Genetic diversity

A total of 34 alleles were recorded for 10 polymorphic loci of the six enzymes analyzed. Appendix C summarizes the
information of allele frequencies recorded. All loci were polymorphic in all populations and the average number of
observed alleles per locus (A) in all populations studied was 3.4 (Table 2). Average observed heterozygosity in wild
population was Ho ¼ 0.556, with a slightly lower value in managed in situ populations (Ho ¼ 0.536) and a slightly higher
value in cultivated populations (Ho ¼ 0.611). Biased and unbiased expected heterozygosity had a similar pattern
(He(b) ¼ 0.580 and He ¼ 0.583 in wild populations; He(b) ¼ 0.574 and He ¼ 0.578 in managed in situ populations;
He(b) ¼ 0.584 and He ¼ 0.588 in cultivated populations). However, none of these differences were statistically significant.
For Ho P ¼ 0.177 (H ¼ 3.467), for He(b) P ¼ 0.875 (H ¼ 0.267), and for He P ¼ 0.875 (H ¼ 0.267).
Fixation indexes (Appendix D electronic version only) indicate that in most loci of all populations the observed
heterozygotes were similar to those expected according to the Hardy–Weinberg equilibrium. Three loci (GOT-2, PGI, and
MNR) from all populations and from the three types of management are in equilibrium. However, significant differences
were identified in seven loci in some populations (Appendix D electronic version only). In seven cases, He was higher than
Ho (in loci EST-2, EST-3 and ACPH-2), and in 14 cases Ho was higher than He, indicating an excess of heterozygotes,
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Table 2
Parameters of genetic diversity in wild, managed in situ and cultivated populations of Stenocereus pruinosus

Population N A P (%) Ho He(b) He

Wild 1 28.00 3.4 100 0.539 0.537 0.546

Wild 2 29.30 3.4 100 0.550 0.571 0.581
Wild 3 28.70 3.4 100 0.579 0.551 0.561
Group W 28.67 3.4 100 0.556 0.580 0.583
Managed in situ 1 28.50 3.4 100 0.540 0.543 0.553
Managed in situ 2 23.00 3.4 100 0.575 0.563 0.575
Managed in situ 3 27.50 3.4 100 0.500 0.558 0.568
Group M 26.33 3.4 100 0.536 0.574 0.578
Cultivated 1 28.80 3.4 100 0.604 0.568 0.579
Cultivated 2 28.10 3.4 100 0.565 0.580 0.590
Cultivated 3 28.90 3.4 100 0.664 0.529 0.538
Group C 28.60 3.4 100 0.611 0.584 0.588

N, sample size; A, mean number of alleles per locus; P, percentage of polymorphic loci; Ho, mean observed heterozygosity (direct counting); He(b), mean
heterozygosity (biased estimate); He, mean heterozygosity (unbiased estimate).

especially in locus MDH in seven populations, followed by the loci GOT-1 in five populations, ACPH-1 in one population,
and EST-1 in one population. Total inbreeding coefficients calculated from average heterozygosity per population were not
significantly different to zero in any population.

3.2. Differentiation of populations

Total genetic diversity averaged at species level was HT ¼ 0.592. It was higher in cultivated populations (HT ¼ 0.585)
than in the wild (HT ¼ 0.575) and in situ managed populations (HT ¼ 0.574). In cultivated populations the highest values of
HT were found in the loci PGI and EST-1 (0.791 and 0.661), whereas the lowest was recorded in locus ACPH-2 (0.320). The
highest value in wild populations was recorded in locus PGI (0.814), and the lowest in ACPH-1 (0.342). In the managed in
situ populations, the highest value was recorded in locus PGI (0.807) and the lowest in ACPH-1 (0.401) (Table 3).
Wild populations had in average HS ¼ 0.522, whereas managed in situ populations had HS ¼ 0.523 and cultivated
populations HS ¼ 0.526. The highest value in all populations was observed in locus PGI (0.760 in cultivated, 0.727 in wild,
and 0.787 in managed in situ populations) and the lowest in locus ACPH-2 (0.315 in cultivated, 0.336 in wild, and 0.336 in
managed in situ populations). Genetic differentiation between populations (DST) was generally low, although slightly
higher in the cultivated populations and lower in the managed in situ populations (Table 3).
The proportion of genetic diversity among populations (GST) was 8.33% for wild populations, whereas 91.67% occurs
within populations. In managed in situ populations 7.99% of variation occurs among populations and 92.01% within
populations. Finally, in cultivated populations 9.04% of variation is distributed among populations and 90.96% within
populations (Table 3).
Total FST value for all populations was 0.064, whereas it was 0.046 in wild populations, 0.035 in managed in situ
populations, and 0.044 in cultivated populations (Table 3), indicating that most of the genetic diversity occurs within
populations and that wild populations are the most differentiated whereas the managed in situ populations are the least
differentiated.
Total estimations of FIS, FIT, and FST are significantly different to zero (Po0.05) in six, six, and nine loci, respectively
(Table 4). FIS statistics show three negative values (excess of heterozygotes) and three positives (excess of homozygotes).
Three FIT values were negative and three were positive. The mean of FIS and FIT indicate significant differences to zero. Most
FST values are significantly different to zero, except in locus MDH. Mean FST was significantly higher than zero (0.064),
indicating that 6.4% of genetic variation is distributed among populations, and therefore most of the genetic variation
occurs within populations (93.6%). FIS values also differ significantly from zero (Po0.001), the mean value 0.023
indicating an excess of heterozygotes.
The average gene flow for all populations was Nm(GST) ¼ 3.80, indicating a high gene flow (Appendix D electronic
version only). Values of Nm(GST) were higher in wild populations (13.510) than in managed in situ populations (7.390)
and in these two population types higher than in cultivated populations (4.240). Trends in Nm(FST) values were similar:
in wild populations Nm(FST) ¼ 5.211, in managed in situ populations Nm(FST) ¼ 6.952, and in cultivated populations
Nm(FST) ¼ 5.473.

3.3. Genetic distance

Cultivated populations C1 and C2 are the most similar populations among themselves (Fig. 1). A second group is
constituted by wild populations W2 and W3 along with the managed populations M1 and M2. The cultivated and managed
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Table 3
Parameters of genetic structure of wild, managed in situ and cultivated populations of Stenocereus pruinosus of the Tehuacán Valley

Parameter Population group Locus

GOT-1 GOT-2 ACPH-1 ACPH-2 MDH EST-1 EST-2 EST-3 PGI MNR Average

HS Wild 0.478 0.456 0.336 0.390 0.602 0.681 0.583 0.624 0.727 0.341 0.522
Managed 0.473 0.589 0.400 0.443 0.599 0.468 0.544 0.575 0.787 0.356 0.523
Cultivated 0.477 0.529 0.466 0.315 0.606 0.604 0.562 0.593 0.767 0.338 0.526
Total 0.476 0.525 0.401 0.382 0.602 0.585 0.563 0.597 0.760 0.648 0.554

DST Wild 0.012 0.039 0.005 0.005 0.001 0.013 0.030 0.037 0.087 0.302 0.053
Managed 0.026 0.020 0.001 0.051 0.017 0.016 0.015 0.005 0.020 0.341 0.051
Cultivated 0.003 0.024 0.016 0.005 0.016 0.056 0.087 0.017 0.024 0.339 0.059
Total 0.024 0.033 0.012 0.030 0.012 0.057 0.057 0.041 0.062 0.052 0.038

HT Wild 0.490 0.495 0.342 0.395 0.603 0.694 0.613 0.661 0.814 0.643 0.575
Managed 0.499 0.609 0.401 0.494 0.615 0.484 0.558 0.579 0.807 0.697 0.574
Cultivated 0.480 0.554 0.482 0.320 0.622 0.661 0.649 0.610 0.791 0.677 0.585
Total 0.500 0.558 0.413 0.412 0.614 0.642 0.620 0.639 0.822 0.700 0.592

GST Wild 0.025 0.078 0.016 0.013 0.001 0.019 0.049 0.056 0.107 0.470 0.083
Managed 0.052 0.033 0.003 0.103 0.027 0.032 0.026 0.008 0.025 0.489 0.080
Cultivated 0.007 0.044 0.034 0.016 0.026 0.085 0.134 0.028 0.030 0.501 0.090
Total 0.049 0.059 0.029 0.073 0.019 0.089 0.092 0.065 0.075 0.075 0.062

Nm(GST) Wild 4.433 1.311 6.899 8.409 103.156 5.781 2.164 1.865 0.929 0.125 13.508
Managed 2.023 3.268 37.390 0.964 3.969 3.321 4.158 14.292 4.346 0.116 7.385
Cultivated 16.438 2.412 3.153 6.674 4.243 1.195 0.720 3.912 3.579 0.111 4.244
Total 3.859 3.140 6.560 2.520 10.243 2.016 1.956 2.858 2.436 2.452 3.804

FST Wild 0.025 0.069 0.016 0.013 0.001 0.019 0.049 0.056 0.107 0.059 0.046
Managed 0.052 0.033 0.003 0.103 0.027 0.032 0.026 0.008 0.025 0.041 0.035
Cultivated 0.007 0.044 0.034 0.016 0.026 0.085 0.134 0.028 0.030 0.010 0.044
Total 0.049 0.056 0.029 0.073 0.019 0.089 0.092 0.065 0.075 0.075 0.064

Nm(FST) Wild 9.970 3.393 15.518 18.920 231.805 13.007 4.868 4.196 2.091 3.990 5.211
Managed 4.554 7.354 84.117 2.169 8.934 7.472 9.358 32.152 9.772 5.802 6.952
Cultivated 37.003 5.427 7.091 15.017 9.549 2.687 1.621 8.801 8.055 23.725 5.457
Total 4.884 4.230 8.302 3.187 12.965 2.551 2.475 3.616 3.083 3.103 3.659

HT, total genetic diversity; HS, genetic variation within populations; DST, genetic variation among populations; GST, genetic differentiation coefficient;
FST, Wright’s statistic of genetic differentiation of populations; Nm(GST) and Nm(FST), parameters estimating gene flow among populations.

Table 4
Wright’s F statistics for polymorphic loci in wild, managed in situ, and cultivated groups of populations of Stenocereus pruinosus in the Tehuacán Valley

Locus Wild Managed in situ Cultivated Total

FIS FIT FST FIS FIT FST FIS FIT FST FIS FIT FST

GOT-1 0.373 0.339 0.025 0.268 0.202 0.052 0.490 0.480 0.007 0.377 0.310 0.049
GOT-2 0.063 0.010 0.069 0.166 0.127 0.033 0.050 0.004 0.044 0.096 0.035 0.056
ACPH-1 0.207 0.188 0.016 0.235 0.231 0.003 0.360 0.314 0.034 0.275 0.238 0.029
ACPH-2 0.064 0.050 0.013 0.255 0.332 0.103 0.012 0.029 0.016 0.080 0.147 0.073
MDH 0.549 0.547 0.001 0.612 0.569 0.027 0.632 0.590 0.026 0.598 0.568 0.019
EST-1 0.122 0.139 0.019 0.061 0.026 0.032 0.037 0.052 0.085 0.019 0.106 0.089
EST-2 0.304 0.338 0.049 0.293 0.311 0.026 0.385 0.467 0.134 0.327 0.389 0.092
EST-3 0.343 0.380 0.056 0.421 0.426 0.008 0.115 0.140 0.028 0.293 0.338 0.065
PGI 0.190 0.277 0.107 0.354 0.370 0.025 0.104 0.131 0.030 0.217 0.276 0.075
MNR 0.018 0.042 0.059 0.126 0.162 0.041 0.086 0.075 0.010 0.008 0.082 0.075

Average 0.006 0.040 0.046 0.031 0.064 0.035 0.093 0.046 0.044 0.023 0.042 0.064

 Po0.01.
 Po0.001.
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0.200 0.150 0.100 0.050 0.000

Cultivated 1

Cultivated 2

Managed in situ 1

Managed in situ 2

Wild 3

Wild 2

Managed in situ 3

Wild 1

Cultivated 3

Fig. 1. Phenogram of genetic distances (based on Nei, 1972) between wild, managed in situ and cultivated populations of Stenocereus pruinosus of the
Tehuacán Valley, México.

in situ populations from Coxcatlán (C3 and M3, respectively), and the wild population from Coatepec (W1) differ relatively
among themselves and even more with the other groups mentioned. No correlation was found through the Mantel test
between genetic and geographic distances (r ¼ 0.116, P40.280).

4. Discussion

4.1. Genetic variation of S. pruinosus

Parameters evaluating genetic diversity of S. pruinosus calculated in this study (A ¼ 3.4, Ho ¼ 0.569, and He ¼ 0.595)
are the highest reported using isozyme analysis among 15 species of columnar cacti studied (Table 5). Genetic
diversity of S. pruinosus is markedly higher than that reported for other species of the genus Stenocereus, including
S. stellatus, a species coexisting with S. pruinosus in Central Mexico and managed in similar ways (Casas et al., 2006,
Table 5). It is also higher than genetic diversity reported for unmanaged species such as Stenocereus gummosus,
Stenocereus eruca, and Stenocereus thurberi from the Sonoran Desert (Clark-Tapia and Molina-Freaner, 2003; Clark-Tapia
et al., 2005; Hamrick et al., 2002). Genetic diversity of S. pruinosus estimated in this study is only lower than that reported
by Otero-Arnaiz et al. (2005a, b) for the columnar cactus P. chichipe, but that study was performed using microsatellite
markers.
A reduction of genetic variation was initially expected in managed in situ and cultivated populations with respect to
wild populations, as commonly found in crop species compared with their wild relatives (Doebley, 1992). This pattern has
been observed in species of columnar cacti such as E. chiotilla (Tinoco et al., 2005) P. chichipe (Lucio, 2005; Otero-Arnaiz
et al., 2005a, b), and P. chende (Ruı́z-Durán, 2007), as well as in most domesticated and incipiently domesticated species
(see Doebley, 1992 for several crop species, Colunga-Garcı́aMarı́n and Zizumbo-Villarreal, 2007; Hughes et al., 2007; Mapes
et al., 1996 for Amaranthus species; Vargas-Ponce, 2007 for Agave species; Zárate et al., 2005 for Leucaena spp.).
But in S. stellatus, a species under more intensity of management, Casas et al. (2006) detected a slight but significant
increase of genetic variation in managed in situ and cultivated populations with respect the wild ones (Table 6). In a
similar way, S. pruinosus shows a slight tendency to decreasing genetic variation in managed in situ populations
and increasing in cultivated populations were detected when compared with wild populations, although these tendencies
were not statistically significant. As in the case of S. stellatus, lower levels of genetic variation in managed in situ
populations with respect to wild populations could be explained because this management involves the removal of part of
the original population and, commonly, the vegetative propagation of the preferred phenotypes. However, the amount of
genetic diversity in managed in situ populations of S. pruinosus is high compared with other species showed in Table 6. For
instance, it is also important to consider managed in situ populations as significant reservoirs.
Similarly to observations made in S. stellatus, high levels of genetic variation in cultivated populations appear to be
determined by the dynamic replacement of individual plants within plantations, including the introduction of vegetative
materials from other villages and even regions. But genetic variation appears to be also favored by tolerance and care of
seedlings and young plants established in homegardens from seeds dispersed by birds, bats and humans. According to this
pattern, intensity of the traditional management appears to favor genetic variation of these incipiently domesticated cacti
species.
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Table 5
Genetic diversity of columnar cacti species estimated through isozyme analysis

Specie A Ho He Management type Reference

Carnegiea gigantea 2.20 0.110 0.116 Wild Hamrick et al. (2002)

Cereus repandus 2.44 0.179 0.205 Wild Nassar et al. (2003)
Escontria chiotilla 1.50 0.065 0.122 Wild, management in situ Tinoco et al. (2005)
Lophocereus schottii 2.33 0.142 0.144 Wild Parker and Hamrick (1992)
Pachycereus pringlei 2.50 * 0.200 Wild Fleming et al. (1998)
Pilosocereus lanuginosus 2.69 * 0.253 Wild Nassar et al. (2003)
Polaskia chende 3.40 0.421 0.542 Wild, management in situ Ruı́z-Durán, 2007
Polaskia chichipe 2.82 0.390 0.458 Wild, management in situ, cultivation Lucio (2005)
Stenocereus eruca 1.48 0.040 0.158 Wild Clark-Tapia et al. (2005)
Stenocereus griseus 2.36 0.145 0.161 Wild, cultivation Nassar et al. (2003)
Stenocereus gummosus 2.00 0.103 0.261 Wild Clark-Tapia and Molina-Freaner (2003)
Stenocereus pruinosus 3.40 0.569 0.595 Wild, management in situ, cultivation This study
Stenocereus thurberi 2.36 0.157 0.169 Wild Hamrick et al. (2002)
Stenocereus stellatus 2.35 – 0.264 Wild, management in situ, cultivation
Weberbauerocereus weberbaueri 2.88 * 0.257 Wild Sahley (1996)

Table 6
Mean7s.e. He in wild, managed in situ and cultivated populations of columnar cacti of the Tehuacán Valley

Species No. of loci Management type

Wild Managed in situ Cultivated

Escontria chiotillaa 13 0.13470.007 0.11070.004 –

Polaskia chichipeb 15 0.43170.043 0.36870.046 0.36970.048
Polaskia chendeb 15 0.53970.043 0.51670.044 –
Stenocereus stellatusc 16 0.25370.016 0.27070.006 0.28970.015
Stenocereus pruinosus 10 0.58370.009 0.57870.006 0.58870.016

In all cases, at least 30 individual plants per population and three populations per management type were analyzed.
a
Tinoco et al. (2005).
b
Blancas et al. (2006).
c
Casas et al. (2006).

4.2. Genetic differentiation of populations

Parameters related to genetic structure of populations reported in Table 3 indicate that most of the genetic variation of
S. pruinosus occurs within populations, and that this proportion is slightly higher in cultivated populations. This
information suggests that efforts in conserving particular populations can be effective in maintaining a high percentage of
the variation, especially in those populations containing higher variation such as populations wild W2, cultivated C1, and
managed in situ M2, which had consistently higher expected heterozygosity (Table 2). It is notorious that in general
cultivated and managed in situ populations are reservoirs of high genetic diversity, which implies that along with
conservation of natural areas within and adjacent the biosphere reserve, in situ conservation of genetic diversity of
S. pruinosus would be greatly benefited with programs of protection and enrichment of the traditional homegardens and
agro-silvicultural systems of the area. In addition, it is also important to consider special measures to protect both
individual plants and populations containing rare alleles. This is for instance the case of allele 3 of locus ACPH-2, the rarest
of all alleles analyzed in this study and which is better represented in the wild population W3 from Coxcatlán. Other
examples are allele 4 of the locus EST-1, which is better represented in the cultivated population C2, allele 2 of PGI in the
managed in situ population M2, and alleles 1 of MNR and 1 of the locus ACPH-1 in the cultivated population C1.

4.3. Gene flow

Values of all parameters estimating gene flow among populations are generally high (total Nm(GST) ¼ 3.804 and
Nm(FST) ¼ 3.659). The highest values of Nm(GST) were documented occurring among wild (13.508) and managed in situ
(7.385) populations, whereas the lowest values were estimated occurring among cultivated populations (4.224). The
highest values of Nm(FST) were documented occurring among managed in situ (6.952) and cultivated populations (5.457),
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whereas the lowest were documented among wild populations (5.211) but in all cases the lowest values were significantly
higher than one. Such high gene flow may be explained in part because the bat L. curasoae is among the main pollinators of
S. pruinosus (Cortés-Dı́az, 1996), and it has been demonstrated to have high mobility, being able to fly nearly 100 km to
forage nectar and pollen in the Sonoran Desert (Horner et al., 1998), whereas the longest distance separating the
populations studied is c. 31 km (Appendix B electronic version only), which makes possible genetic interactions between so
distanced populations. However, it is important to point out that it has not been evaluated what effective distances
pollinator bats fly in the Tehuacán Valley, how frequent are long distance flights and whether Stenocereus pollen may
survive those flights. Gene flow is also determined by seed dispersers, mainly birds and bats which are effective for long
distance dispersion. In addition, humans participate actively in dispersing both seeds and vegetative propagules within
managed areas, and commercialization of fruit in regional markets. Farmers also exchange vegetative propagules among
friends and relatives, favoring long distance dispersion of S. pruinosus. The low values of inbreeding (FIS ¼ 0.023), the low
differentiation of populations (total FIT ¼ 0.042 and FST ¼ 0.064) and the high values of gene flow among all populations are
all indicators of the high efficiency of bats, birds and humans to move pollen, seeds and vegetative propagules among the
studied populations.
Hence, high gene flow occurring among all populations might explain why genetic variation within managed in situ and
cultivated populations is as high as in wild populations. Also, this high gene flow explains why differentiation of
populations is low even when artificial selection is operating actively favoring individual phenotypes producing better
fruit. All this information leads us to consider that all populations studied could be part of a larger metapopulation in the
region. In other words, gene flow seems to be continually counteracting the effect of artificial selection on managed in situ
and cultivated populations and for this reason the system is maintained within a state of incipient domestication or
semidomestication (Clement, 1999; Pickersgill, 2007). It is possible to predict that in the absence of artificial selection
associated to human cultural change in relation to valuing this plant resource, differences between populations resulting
from the process of domestications would be lost. Similarly, limitations to gene flow due to scarcity or absence of wild
populations and/or scarcity or absence of pollinators and seed dispersers would determine higher differentiation among
populations and probably a reduction of the genetic variation contained within homegardens and agro-silvicultural
systems.

4.4. Genetic distances

The phenogram of Fig. 1 shows that the pairs of populations composed by the cultivated populations C1 and C2, the
managed in situ M1 and M2, and the wild ones W2 and W3 are more similar among them. Such trend indicates that
populations are genetically more similar among them in relation to management rather than in relation to the geographic
distance, which is different to the trend found in other columnar cacti species managed in the region such as E. chiotilla
(Tinoco et al., 2005), P. chichipe (Otero-Arnaiz et al., 2005a, b), and S. stellatus (Casas et al., 2006), in which geographic
distance was found to be more relevant than management type to explain genetic distance. Differences in this trend with
E. chiotilla and P. chichipe could be explained in part because these species are pollinated mainly by bees (Oaxaca-Villa et al.,
2006; Otero-Arnaiz et al., 2003, respectively), and because these species are less intensely managed than S. pruinosus. But
in the case of S. stellatus, species in which both pollinators and seed dispersers are similar to those of S. pruinosus, the main
difference is in management intensity, which is higher in S. pruinosus. It is possible that such difference explains why
genetic distance is more influenced by management type. Nevertheless, it is also important to consider that values of
genetic distance in all cases are generally low, as it would be expected in a species whose populations of domesticated and
wild relatives coexist and interchange genes dynamically as it is the case of the system studied.

4.5. Traditional management and conservation

Patterns of population genetics and their relation to traditional management documented in this study are generally
similar to those reported by Casas et al. (1999a–c) for S. stellatus, who described the high efficacy of traditional
management in the maintenance of genetic variation of that species of columnar cactus. When comparing the Stenocereus
species among them and with other columnar cacti it appears that as traditional management intensifies, the capacity of
maintaining genetic diversity in artificial systems increases. This is an atypical pattern since, as mentioned, it is more
common to find lower genetic variation in domesticated artificial systems compared with populations of wild relatives
(see for instance Doebley, 1992). Clearly, traditional management of agricultural systems and domestication of plants is
based on the interest of local people for favoring the best phenotypes of plants according to utilitarian purposes, and
artificial selection is therefore practiced in this direction. But traditional artificial selection is directed to favor not one or
few but multiple variants according to the pattern of multiple uses of resources and ecosystems traditionally practiced by
Mesoamerican peoples (Toledo et al., 2002). In this way, although artificial selection in a given moment causes a reduction
of genetic diversity favoring particular variants, throughout time it is capable to accumulate similar or more genetic
variation than that of natural populations. In the case of S. stellatus, for instance, Casas et al. (1997) documented that local
people of the Tehuacán Valley favor variants producing fruits with spiny not red peel which are efficient to prevent
frugivorous attack, but they also favor variants producing fruit less spiny which are easier to manipulate. Similarly, people
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2006 F. Parra et al. / Journal of Arid Environments 72 (2008) 1997–2010

may favor variants producing fruit with thick peel which are more resistant for storing and transportation, but also they
use to favor variants producing fruit with thin peel which are easier to handle for direct consumption and to produce dry
fruit. People may also favor variants producing fruit with sweet flavor which are better for consumption as fresh fruit, but
also they may favor variants producing fruits with bittersweet flavor which are better to manufacture other edible
products. Finally, people may favor variants producing fruits with pulp of different colors simply because of their pleasure
to appreciate them or because their flavors are different. Selection of all these contrasting phenotypes might therefore
derive in the accumulation of high genetic diversity.
S. pruinosus is a species appreciated by people in the region, with high cultural and economic value that favors its
management and the interest for conserving its diversity (Casas et al., 1999a–c). The traditional systems are efficient in
maintaining diversity just because of the cultural and economic value of the resources and, therefore, incentives for
enhancing such value have great importance in designing strategies for conservation of genetic diversity of this and other
species similarly managed and valued. Enhancing of traditional practices such as the interchange of seeds and vegetative
propagation material from wild and other cultivated and/or managed in situ populations from other villages or regions
have particular importance for the purposes of conserving genetic resources and developing domestication processes of
S. pruinosus and other native plant species under processes of domestication. Losing these practices would decrease genetic
variation. S. pruinosus forms part of traditional agricultural systems such as homegardens and agro-silvicultural systems
whose future maintenance has important risks. For instance, Casas et al. (2006) and Farfán-Heredia (2006) have
documented that the agro-silvicultural systems of the region have been progressively abandoned and substituted by
agricultural systems that eliminate the vegetation cover. Similarly, Carmona and Casas (2005) and Blancas (2007)
documented that cultivation of P. chichipe and that use and cultivation of Myrtillocactus schenckii, respectively, have been
gradually abandoned in the Tehuacán Valley. Consequently, the permanence of these systems and their cultural and
economic incentives, along with preservation of natural vegetation, are crucial for conserving genetic resources of this and
other species and to maintain ongoing the process of their domestication.

Acknowledgements

The authors thank DGAPA, UNAM (research projects IN220005 and IN219608), SEMARNAT/CONACYT, Mexico (research
project 2002-C01-0544), and Royal Gardens, Kew, for financial support, as well as Edgar Pérez-Negrón for field work
assistance, people of the villages of the study area, who kindly allowed us to work in their land, and two anonymous
reviewers for their valuable suggestions to improve the manuscript.
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Appendix A

Localization of the Tehuacán Valley in the status of Puebla and Oaxaca in Central Mexico and the studied populations of
Stenocereus pruinosus. W, wild populations; M, managed in situ populations; C, cultivated populations.
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Appendix B. Geographic distances (km) between the wild (W), managed in situ (M), and cultivated (C) populations of
S. pruinosus studied

WI WII WIII MI MII MIII CI CII CIII

WI *
WII 1.8 *
WIII 27.5 28.8 *
MI 9.3 10.0 30.5 *
MII 2.0 3.3 27.5 7.5 *
MIII 25.8 26.8 5.0 27.0 25.3 *
CI 8.8 8.8 31.3 1.8 7.5 28.3 *
CII 5.0 6.3 28.3 7.5 3.8 24.5 3.8 *
CIII 25.0 26.8 8.8 25.5 25.0 4.3 27.0 24.3 *

Appendix C. Allele frequencies for the 10 loci analyzed in wild (W), managed in situ (M), and cultivated (C)
populations of S. pruinosus in the de Tehuacán Valley, Mexico

Locus Population

Allele W1 W2 W3 M1 M2 M3 C1 C2 C3

Got-1 1 0.400 0.350 0.533 0.569 0.542 0.315 0.650 0.600 0.552
2 0.600 0.650 0.467 0.431 0.458 0.685 0.350 0.400 0.448

Got-2 1 0.200 0.008 0.067 0.067 0.271 0.155 0.133 0.283 0.083
2 0.667 0.450 0.717 0.650 0.396 0.466 0.700 0.583 0.533
3 0.133 0.467 0.217 0.283 0.333 0.379 0.167 0.133 0.383

Acph-1 1 0.083 0.052 0.067 0.083 0.109 0.103 0.317 0.067 0.150
2 0.850 0.741 0.800 0.783 0.717 0.759 0.617 0.750 0.683
3 0.067 0.207 0.133 0.133 0.174 0.138 0.067 0.183 0.167

Acph-2 1 0.207 0.100 0.115 0.155 0.167 0.500 0.083 0.140 0.117
2 0.690 0.817 0.769 0.741 0.786 0.431 0.833 0.740 0.867
3 0.103 0.083 0.115 0.103 0.047 0.069 0.083 0.120 0.017

Mdh 1 0.267 0.283 0.276 0.133 0.354 0.286 0.367 0.267 0.150
2 0.217 0.167 0.190 0.350 0.146 0.179 0.133 0.217 0.350
3 0.517 0.550 0.535 0.517 0.500 0.536 0.500 0.517 0.500

Est-1 1 0.214 0.093 0.183 0.167 0.083 0.035 0.383 0.150 0.121
2 0.321 0.389 0.433 0.717 0.604 0.759 0.317 0.433 0.759
3 0.304 0.463 0.283 0.033 0.250 0.172 0.150 0.217 0.069
4 0.161 0.056 0.100 0.083 0.063 0.035 0.150 0.200 0.052

Est-2 1 0.140 0.400 0.104 0.261 0.167 0.250 0.182 0.273 0.220
2 0.620 0.400 0.542 0.544 0.738 0.521 0.523 0.568 0.120
3 0.240 0.200 0.354 0.196 0.095 0.229 0.296 0.159 0.660

Est-3 1 0.341 0.483 0.250 0.411 0.500 0.500 0.259 0.308 0.074
2 0.227 0.367 0.517 0.464 0.386 0.460 0.483 0.519 0.574
3 0.432 0.150 0.233 0.125 0.114 0.040 0.258 0.173 0.352

Pgi 1 0.417 0.183 0.100 0.083 0.104 0.069 0.083 0.167 0.241
2 0.033 0.167 0.083 0.067 0.188 0.121 0.133 0.083 0.086
3 0.350 0.033 0.033 0.283 0.167 0.311 0.067 0.150 0.241
4 0.117 0.167 0.033 0.250 0.104 0.293 0.317 0.300 0.086
5 0.067 0.217 0.300 0.200 0.333 0.138 0.367 0.283 0.259
6 0.017 0.233 0.450 0.117 0.104 0.069 0.033 0.017 0.086

Mnr 1 0.135 0.093 0.089 0.039 0.087 0.115 0.204 0.125 0.067
2 0.115 0.185 0.232 0.289 0.261 0.096 0.093 0.125 0.233
3 0.731 0.426 0.429 0.500 0.326 0.327 0.241 0.268 0.233
4 0.019 0.296 0.250 0.173 0.326 0.462 0.463 0.482 0.467
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Appendix D. Fixation indexes (F) per polymorphic locus in wild (W), managed in situ (M), and cultivated (C)
populations of S. pruinosus

Locus Population

WI WII WIII MI MII MIII CI CII CIII

** * * *
GOT-1 0.093 0.513 0.449 0.451 0.315 0.073 0.225 0.366 0.781***
GOT-2 0.185 0.256 0.281 0.197 0.009 0.267 0.059 0.183 0.225
ACPH-1 0.109 0.255 0.164 0.178 0.247 0.202 0.464** 0.231 0.290
ACPH-2 0.064 0.037 0.186 0.185 0.077 0.455** 0.011 0.063 0.024
MDH 0.546*** 0.502 0.519** 0.604*** 0.623*** 0.521*** 0.645 0.546*** 0.625***
EST-1 0.234 0.124 0.048 0.273 0.235 0.123 0.158** 0.067 0.074
EST-2 0.272 0.385* 0.285 0.360 0.468** 0.487 0.461** 0.218
EST-3 0.450** 0.301 0.308 0.532*** 0.547*** 0.197 0.304 0.315 0.276
PGI 0.042 0.270 0.286 0.172 0.280 0.650 0.242 0.236 0.109
MNR 0.216 0.102 0.037 0.009 0.283 0.139 0.073 0.050 0.176
Populational F 0.014 0.052 0.032 0.023 0.001 0.120 0.044 0.043 0.235

Significant deviations with respect the expected values are indicated by asterisks. *Po0.05, **Po0.01, ***
Po0.001.

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