This article was published in an Elsevier journal. The attached copy
is furnished to the author for non-commercial research and
education use, including for instruction at the author’s institution,
sharing with colleagues and providing to institution administration.
Other uses, including reproduction and distribution, or selling or
licensing copies, or posting to personal, institutional or third party
websites are prohibited.
In most cases authors are permitted to post their version of the
article (e.g. in Word or Tex form) to their personal website or
institutional repository. Authors requiring further information
regarding Elsevier’s archiving and manuscript policies are
encouraged to visit:
http://www.elsevier.com/copyright
Author's personal copy
Available online at www.sciencedirect.com
Forest Ecology and Management 255 (2008) 334–339
www.elsevier.com/locate/foreco
Genetic (AFLP) diversity of nine Cedrela odorata populations
in Madre de Dios, southern Peruvian Amazon
Amanda de la Torre a,*, Cesar López a, Eliana Yglesias a, Jonathan P. Cornelius b
a
Universidad Nacional Agraria La Molina, Av. La Universidad s/n La Molina, Lima 12, Peru
b
World Agroforestry Centre, CIP-ICRAF, Apartado 1558, Lima 12, Peru
Abstract
Cedrela odorata L., one of the most important neotropical timber species, is threatened by deforestation and unsustainable logging in many
parts of its natural range. Information on patterns of genetic variation is useful in informing both reforestation and genetic conservation activities.
However, to date, no such information is available in Peru or elsewhere in South America. In the present study, genetic diversity between and within
nine Peruvian populations of the species, based on amplified fragment length polymorphism (AFLP) markers, is reported. Overall diversity level
was high (Ht = 0.22), as expected for a widespread, long-lived tropical species, and consistent with previous studies carried out in Central America.
Levels of intrapopulation diversity were higher than those previously reported for the species (Hs = 0.13–0.21). Analysis of molecular variation
revealed genetic differences between two population groups located on different rivers and between populations located on the same rivers.
Differences between groups were greater than those within groups. Genetic and geographical distances were significantly correlated. The relatively
strong genetic differences between populations may be related to the riparian, essentially one-dimensional spatial distribution pattern of the
populations studied. No difference was found in percentage of polymorphic loci between relatively undisturbed and logged populations. The
existence of appreciable genetic differentiation over a relatively small part of the species range in the Peruvian Amazon suggests the need for
caution in use of seed outside its zone of origin. For genetic conservation purposes, it would probably be prudent to sample (ex situ) or conserve (in
situ) populations in each of the major watersheds of the Peruvian Amazon.
# 2007 Elsevier B.V. All rights reserved.
Keywords: Meliaceae; Forest genetic resources; Genetic conservation
1. Introduction
Cedrela odorata L. (cedro, Spanish cedar) is a neotropical,
broadleaf tree species. Its broad, transequatorial distribution
extends from 268N in Mexico to 288S in northern Argentina,
and includes moist and seasonally dry forest types, and
altitudes ranging from sea level to 1200 m a.s.l. (Pennington
and Styles, 1975). The timber of C. odorata, like that of other
Swietenioideae (e.g. the American mahoganies, Swietenia
spp.), is of high value and is much in demand on domestic and
international markets. It is classed as ‘vulnerable’ by IUCN
and is threatened both by unsustainable logging (IUCN, 1994;
Patiño, 1997) and by forest conversion to pasture and other
land uses. In Peru, Spanish cedar is considered a threatened
* Corresponding author at: Centre for Forest Conservation Genetics,
University of British Columbia, 3041-2424 Main Mall, Vancouver, B.C.,
Canada V6T 1Z4. Tel.: +51 1 4366804.
E-mail address: amandaro@interchange.ubc.ca (A. de la Torre).
0378-1127/$ – see front matter # 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.foreco.2007.09.058
species by national authorities (INRENA, 2004) and since
1988 has been listed on CITES Appendix III, under which
both export and import require export permits from the
producing country (CITES, 2004). However, the species
remains relatively common in many parts of its range
(including parts of the Peruvian Amazon), including
agricultural landscapes, where its heliophytic status and
nurturing by farmers appear to have helped to ensure its
continued presence in fencerows and forest remnants. In
Madre de Dios province, southern Peruvian Amazon, where
the present study was carried out, many remaining populations of C. odorata are riparian, i.e. located close to main
rivers or to oxbow lakes. Because of their accessibility (i.e.
via navigable rivers), many populations in the zone have been
heavily depleted.
Effective conservation and use of this and other vulnerable
species depends partially on knowledge of patterns of genetic
variation. For example, the spatial structure of genetic variation
should inform sampling strategies for ex situ or in situ
conservation. Similarly, marked between-population genetic
Author's personal copy
A. de la Torre et al. / Forest Ecology and Management 255 (2008) 334–339
differentiation would indicate the need for caution – at least – in
use of seed for planting outside its area of origin. This applies
even to neutral genetic variation detected by molecular
markers, as differentiation may indicate relative absence of
migration, which in turn could permit the development of
variation in adaptive traits that otherwise could be prevented by
gene flow.
In the case of Spanish cedar, studies by Gillies et al. (1997),
Cavers et al. (2003a) and Navarro (2002) have revealed
pronounced genetic differences between populations from the
Pacific and Atlantic regions of Costa Rica. However, no
information is available for C. odorata in South America,
although the region harbours most of the unlogged populations
of the species.
In the present study, we address two research questions of
relevance to the management of Peruvian C. odorata genetic
resources. First, we look at the degree of genetic differentiation
between populations and between two population groups.
Second, we examine whether there is any indication that human
disturbance, i.e. logging, has to date affected genetic diversity
of intervened populations. In particular, we were interested in
examining whether the most highly intervened populations
would show lower degrees of polymorphism, due to population
bottlenecks (caused by logging) and consequent founder
effects. The presence of such effects would imply that heavily
logged populations should receive lower prioritization in ex situ
and in situ conservation.
In order to address these questions, we present information
on genetic structure and variation in nine populations of the
species. We based our estimates on amplified fragment length
polymorphism (AFLP) markers. AFLPs are suitable markers
for genetic diversity studies as, although dominant, they permit
the assay of a large number of loci.
335
2. Materials and methods
2.1. Study sites and sampling
Populations were sampled in two protected areas: Manu
National Park (six populations) and Los Amigos Conservation
Area (three populations) (Fig. 1 and Table 1). The Manu
populations are located along an approximately 150 km stretch
of the River Madre de Dios. Each population represents an area
of 30–450 ha where the species occurs at variable, relatively
high densities, i.e. 0.3–7 trees ha 1 (Table 1). With the
exception of one additional, unsampled population (Cocha
Juárez), located between Otorongo and Limonal populations,
there are no other significant concentrations of the species
either in riparian locations between the sampled populations, or
in adjacent non-riparian locations, although it is probable that
isolated trees or small groups of trees occur in both situations.
We concentrated on riparian populations because, as a common
type, their conservation status is important to the continued
persistence of the species in Madre de Dios. In addition, they
are and have been vulnerable to logging (legal and illegal).
The Los Amigos populations are located 0–43 km upstream
of the confluence of the Madre de Dios and the Amigos rivers,
which occurs approximately 217 km downstream of the closest
of the Manu populations. The intervening stretch of the River
Madre de Dios flows through heavily deforested areas. In terms
of human intervention, the populations fall into two groups: the
Los Amigos populations and Limonal in Manu (located close to
the park boundary) have been intensively logged. Most wellformed trees have been removed, leaving only low density
stands (Table 1) of C. odorata individuals. The remaining
populations are relatively undisturbed, including two (Cashu
and Maizal) that have never been logged.
Fig. 1. Location of nine populations in two groups sampled in a study of genetic diversity of Cedrela odorata in the Southern Peruvian Amazon. Populations are
represented by black dots and located as follows: from the top on the left side: Maizal, Cashu, Gallareta, Salvador, Otorongo and Limonal in Manu; from the bottom on
the right side: Cicra TB, Cicra TA and Pv2 in Los Amigos area.
Author's personal copy
336
A. de la Torre et al. / Forest Ecology and Management 255 (2008) 334–339
Table 1
Description of collection areas sampled in a study of genetic variation of
Cedrela odorata populations in the southern Peruvian Amazon
2.3. Data analysis
Leaf material was collected from a total of 153 individuals
from the nine populations from October to December of 2003;
9–20 individuals were sampled per population (Table 1).
Samples were stored in resealable plastic bags with 10–20 g of
self-indicating silica gel, following Chase and Hills (1991).
Allele frequencies were estimated using the Bayesian method
with non-uniform prior distribution of allele frequencies, as
described by Zhivotovsky (1999). We estimated the degree of
genetic differentiation between groups (i.e. populations on the
River Madre de Dios and those on the River Amigos) and
between populations-within-groups using analysis of molecular
variance (AMOVA) from ARLEQUIN version 3.0 (Excoffier
et al., 2005) and by estimating values of Nei’s F st (Nei, 1973) and
related statistics using the AFLP-SURV software (Vekemans
et al., 2002), following Lynch and Milligan’s (1994) approach.
We tested for a relationship between pairwise physical and
genetic distances (Nei, 1972) between the populations by
estimating values of Spearman’s rank correlation. Genetic
distances were calculated using AFLP-SURV.
In order to test for effects on genetic diversity of population
bottlenecks caused by logging, we examined the relative
degrees of polymorphism of the two groups (logged and
unlogged populations), specifically with regard to expectations
that the most highly intervened populations would show lower
degrees of polymorphism. We did not compare gene diversity
between the two groups, because gene diversity is expected to
be relatively little affected by bottlenecks (because rare alleles
– which are those that are expected to be lost – contribute little
to total heterozygosity).
2.2. Laboratory procedures
3. Results
Total genomic DNA was extracted using the CTAB method
(Doyle and Doyle, 1987). AFLP protocol followed the standard
procedure described by Vos et al. (1995). High quality DNA
(i.e. not damaged and free of impurities) was digested using
restriction enzymes EcoRI and MseI. DNA fragments were
ligated to EcoRI and MseI adapters to generate template DNA
for amplification. PCR was performed in two consecutive
reactions, according to the Invitrogen protocol (Invitrogen,
2003). In the preamplification, genomic DNAs were amplified
with AFLP primers, each having one selective nucleotide. The
PCR products of the amplification reaction were diluted and
used as a template for the selective amplification using two AFLP
primers, each containing three selective nucleotides. Seven
primer combinations were probed: EcoRI-ACT/MseI-CAT;
EcoRI-AAC/MseI-CAC; EcoRI-ACC/MseI-CAT; EcoRIACC/MseI-CTT; EcoRI-ACC/MseI-CAG; EcoRI-ACA/MseICTC; EcoRI-AGG/MseI-CTC. Those with the best resolution
and the greatest number of bands were selected. Thermal cycling
conditions for amplification were optimised to 14 cycles of 94 8C
for 30 s (denaturation), 65 8C for 30 s (annealing) and 72 8C for
60 s (extension); followed by 23 cycles of 94 8C for 30 s, 56 8C
for 30 s, and 72 8C for 60 s. Final temperature was 4 8C.
Amplification products were separated on 6% polyacrylamide
gels, stained with AgNO3 (according to the standard procedure
described by Creste et al., 2001) and visualized through UV light
exposure. Subsequently, the gels were recorded using a camera
and a scanner before scoring the presence or absence of each
scorable band in a binary data matrix.
3.1. General
Collection area
Mean annual
precipitation (mm year 1)
Mean annual
temperature (8C)
Number of
measured trees
Number of
sampled trees
Mean (range) of
densities (trees ha 1)
Number of sampled populations
Number of individuals
sampled per population
Degree of disturbance
Manu
Los Amigos
2500
2845
23
22
540
61
103
50
0.85 (0.3–7)
0.09
(0.05–0.1)
3
13–16
6
9–20
Undisturbed
(except Limonal
population)
Intensively
logged
Three of the seven screened AFLP combinations were used in
the study (of the others, two were rejected because of low
resolution and two because of low numbers of bands). The three
AFLP primer combinations produced a total of 258 bands in 137
individuals (from a total of 153 sampled, 137 were successfully
amplified (Table 2)), of which 255 (98.8%) were polymorphic
(Table 3). The percentage of polymorphism across the nine
populations ranged from 41.5% (Salvador) to 66.7% (Otorongo)
(Table 2). Levels of genetic diversity within populations (Hs)
ranged from 0.13 (Maizal) to 0.21 (Otorongo) (Table 3). Overall
gene diversity (Ht) was estimated at 0.22 and overall F st was 0.20.
3.2. Genetic differentiation
The AMOVA indicated the presence of significant genetic
variation both between the two groups and between populaTable 2
Number of loci evaluated for each of three AFLP primer combinations utilized
in assays of 137 individuals of Cedrela odorata from nine southern Peruvian
Amazon populations
Primer combination
Number of loci
EcoRI-ACT/MseI-CAT
EcoRI-AAC/MseI-CAC
EcoRI-ACC/MseI-CAT
103
97
58
Total
258
Author's personal copy
337
A. de la Torre et al. / Forest Ecology and Management 255 (2008) 334–339
Table 3
Estimated percentage of polymorphic loci (P) and gene diversity (Hs) within nine populations of Cedrela odorata from the southern Peruvian Amazon
Collection area
Population
Manu
Maizal
Cashu
Gallareta
Otorongo
Salvador
Limonal
Los Amigos
PV2
CicraTA
Cicra TB
Sample size
Total
Number of polymorphic loci
P
Hs (S.D.)
18
20
15
13
19
9
112
115
111
172
107
126
43.4
44.6
43
66.7
41.5
48.8
0.13
0.18
0.16
0.21
0.17
0.18
13
14
16
135
120
117
52.3
46.5
45.3
0.17 (0.01)
0.18 (0.01)
0.18 (0.01)
137
255
98.8
0.17 (0.007)
(0.01)
(0.01)
(0.01)
(0.01)
(0.01)
(0.01)
Table 4
Analysis of molecular variance (AMOVA) between two population groups and nine populations-within-groups of Cedrela odorata from the southern Peruvian
Amazon
Source of variation
d.f.
Sum of squares
Variance component
Between groups
Between populations-within-groups
Within populations
1
7
128
367.675
503.09
2830.504
5.01412
3.28699
22.11332
Total
136
3701.272
30.41442
a
Total variance (%)
16.48
10.80
72.70
pa
<0.0001
<0.0001
<0.0001
100
Probability of a higher value of F, based on permutation test (1000 permutations).
tions-within-groups. Almost three-quarters of the variation
(72.7%) was concentrated within populations, while the
between-group component (16.5%) was larger than the
between population-within-group component (10.8%)
(Table 4). Values of F st for populations-within-groups were
similar (0.14 for Manu and 0.15 for Los Amigos) (Table 5).
Overall F st was higher (0.20). The correlation between genetic
and geographic distance was positive and highly significant
(rs = 0.75, p < 0.0005, one-tailed) (Fig. 2).
3.3. Polymorphism in logged and unlogged populations
The percentage of polymorphic loci per population varied
from 43 to 66.7%. The least disturbed populations were not
amongst the most variable and the logged populations had
percentages of polymorphic loci similar to or greater than all
the other populations except the most variable (Otorongo).
(Ht = 0.27, P = 84.8% (Cavers et al., 2003b); Ht = 0.34,
P = 93.8% (Gillies et al., 1997)). However, diversity within
populations, varying from 0.13 to 0.21, was higher than
reported elsewhere. For example, Cavers et al. (2003b) found
that diversity within Costa Rican populations ranged from 0.03
to 0.13. Furthermore, the proportion of polymorphic loci per
population was greater than previously evaluated (41.5–66.7%
vs. 9–22% found by Cavers et al., 2003b).
Either or both of two factors could explain this. First, it
might reflect a South American origin of the species (as
postulated by Cavers et al., 2003a). This would imply a more
recent colonization of Central America, and lower diversity
levels could then be explained by founder effects or population
bottlenecks during migration events (Rivera-Ocasio et al.,
2002; Cavers et al., 2003a,b).
4. Discussion
Overall levels of genetic diversity (Ht = 0.22, P = 98.8%)
were similar to values reported for C. odorata in Mesoamerica
Table 5
Estimates of fixation index (Fst), total gene diversity (Ht) and within population
gene diversity (Hs) for two population groups of Cedrela odorata from Madre
de Dios, southern Peruvian Amazon
Collection area
Hs
Ht
Fst
Manu
Los Amigos
0.17
0.17
0.20
0.21
0.14
0.15
0.22
0.20
Total (all populations)
Fig. 2. Scatter plot of genetic distances and geographic distances between nine
populations of Cedrela odorata located in Madre de Dios, southern Peruvian
Amazon.
Author's personal copy
338
A. de la Torre et al. / Forest Ecology and Management 255 (2008) 334–339
Second, it might reflect different levels of disturbance and
human-induced fragmentation, both of which tend to be much
greater in Central American populations than in the populations studied here, and may have been sufficiently severe to
have led to genetic erosion. Our results, by contrast, indicate
that the degree of disturbance and fragmentation found in the
studied populations has not resulted in genetic erosion. This
probably reflects ongoing gene-flow between the study
populations, from upstream intact populations and from other
trees in non-riparian situations (because gene flow could
restore to individual populations any alleles lost in bottlenecks). Alternatively, it may simply imply that logging
intensity was not sufficiently high to cause measurable founder
effects.
Similar results, attributed to similar causes (i.e. fragmentation, logging and lower long-term effective population sizes),
were found by Lemes et al. (2003) and Novick et al. (2003) for
Central American and Amazonian populations of big-leaf
mahogany (Swietenia macrophylla King), another winddispersed, insect-pollinated, widespread meliaceous species
subject to unsustainable intensive logging.
According to Yeh’s (2000) criteria our findings on genetic
structure indicate large (0.15 < F st 0.25) genetic differentiation at the overall level, and moderate to large (0.05 <
F st 0.15) differentiation at the within-group level. It is
possible that the presence of appreciable genetic differentiation
over this relatively small area may be due to the riparian,
essentially one-dimensional spatial distribution pattern of the
populations studied here. The positive relationship between
genetic and geographical distances suggests that gene flow is
likely to be predominantly between adjacent populations,
corresponding to Kimura and Weiss’s (1964) stepping stone
model. Under the one-dimensional stepping-stone model –
appropriate for these linear, riparian populations – more gene
flow per generation is required to maintain overall panmixia
than in Wright’s (1931) Island Model. For example, in a
stepping stone system with migration rates of 0.1 and 2 10 5,
respectively for adjacent and long-distance gene flow, ‘considerable’ local differentiation will occur if Ne < 100 (Kimura
and Weiss, 1964). In addition, the more pronounced betweengroup variation could not be solely due to greater distance, but
also to barriers to hydrochory-mediated gene flow (because the
two groups are located upstream of the confluence of their
respective rivers). However, based on our data, we cannot
separate such effects from those related purely to isolation by
distance.
Cavers et al. (2003b) reported estimates of fst (an analogue
of F st, based on partitioning of molecular variance between and
within populations (Excoffier et al., 1992)) for two population
groups of C. odorata located in Costa Rica. Our estimates of F st
are similar to the fst estimate from Cavers et al.’s first
population group of (fst = 0.20). The values we report are much
lower than those for Cavers et al.’s (2003b) second group
(fst = 0.47). This, however, covered a larger geographic area
than that sampled here, including populations physically and
reproductively separated by the Costa Rican Central Mountain
range.
Taken together, our results and those of Cavers et al. (2003b)
appear to indicate that C. odorata may have a tendency towards
developing relatively marked differentiation between populations. In part, this could be due to factors specific to the two
study sites (riparian distribution in Madre de Dios, human
intervention in the case of Costa Rica (see above)). However, it
should also be noted that, in general, abiotically dispersed
tropical tree species tend to show relatively large population
differentiation (Loveless, 1992), i.e. this tendency may be due
in part to intrinsic characteristics of the species, and not simply
to local ecological or historical factors.
The presence of relatively pronounced genetic variation
between these relatively closely distributed populations of C.
odorata suggests the need for caution in the use of seed outside
its zone of origin. This would apply particularly in the case of
seed transfers over larger distances than those studied here. The
Peruvian Amazon is a vast region, variable in soil types,
elevations, and amount and distribution of precipitation. These
distances may permit more substantial genetic differentiation
than those observed here (as, indeed, seen in Cavers et al.’s
(2003b) second group (see above)), particularly if reinforced by
a tendency towards linear distributions and, possibly, unidirectional hydrochory. For genetic conservation purposes, it would
probably be prudent to sample (ex situ) or conserve (in situ)
populations in each the major watersheds of the Peruvian
Amazon (e.g. those draining to the Napo, Marañon, Huallaga,
Ucayali and Madre de Dios rivers). Our results suggest that
logged populations should not be excluded from any such
measures, as they do not show signs of being genetically
depauperate. Future research should seek to clarify genetic
structure at these larger geographic scales. Studies of adaptive
variation, preferably of traits of commercial significance,
should also be undertaken, in order to clarify the implications
for planting programmes.
Acknowledgments
This work forms part of the senior author’s MSc thesis and
was done with financial support from ACA (Amazon
Conservation Association) and ICRAF (World Agroforestry
Centre) through competitive grants for 2003.
References
Cavers, S., Navarro, C., Lowe, A.J., 2003a. Chloroplast DNA phylogeography
reveals colonization history of a Neotropical tree Cedrela odorata L. in
Mesoamérica. Mol. Ecol. 12, 1451–1460.
Cavers, S., Navarro, C., Lowe, A.J., 2003b. A combination of molecular
markers identifies evolutionarily significant units in Cedrela odorata L.
(Meliaceae) in Costa Rica. Conserv. Genet. 4, 571–580.
Chase, M., Hills, H., 1991. Silica gel: an ideal material for field preservation of
leaf samples for DNA studies. Taxon 40, 215–220.
CITES, 2004. Listed species database. http://www.cites.org/eng/resources/species.html.
Creste, S., Tulmann, N., Figueira, A., 2001. Detection of single sequence repeat
polymorphisms in denaturing polyacrilamide sequencing gels by silver
staining. Plant Mol. Biol. Rep. 19, 299–306.
Doyle, J.J., Doyle, J.L., 1987. Isolation of plant DNA from fresh tissue. Focus
12, 13–15.
Author's personal copy
A. de la Torre et al. / Forest Ecology and Management 255 (2008) 334–339
Excoffier, L., Smouse, P.E., Quattro, J.M., 1992. Analysis of molecular variance
inferred from metric distances among DNA haplotypes: application to
human mitochondrial DNA restriction data. Genetics 131, 479–491.
Excoffier, L., Laval, G., Schneider, S., 2005. Arlequin ver 3.0: An integrated
software package for population genetics data analysis. Evol. Bioinform.
Online 1, 47–50.
Gillies, A., Cornelius, J., Newton, A., Navarro, C., Hernandez, M., Wilson, J.,
1997. Genetic variation in Costa Rican populations of Spanish Cedar. Mol.
Ecol. 6, 1133–1145.
INRENA, 2004. Lista de especies de flora bajo categorı́a de amenaza. http://
www.inrena.gob.pe.
Invitrogen, 2003. AFLPAnalysis System I, AFLP Starter Primer Kit. Instruction
Manual.
IUCN, 1994. Americas Regional Workshop (Conservation & Sustainable
Management of Trees, Costa Rica) 1998. Cedrela odorata. In: 2004 IUCN
Red List of Threatened Species. http://www.redlist.org/.
Kimura, M., Weiss, G.H., 1964. The stepping stone model of population structure
and the decrease of genetic correlation with distance. Genetics 49, 561–576.
Lemes, M., Gribel, R., Proctor, J., Grattapaglia, D., 2003. Population genetic
structure of mahogany (Swietenia macrophylla King, Meliaceae) across the
Brazilian Amazon, based on variation at microsatellite loci: implications for
conservation. Mol. Ecol. 12, 2875–2883.
Loveless, M.D., 1992. Isozyme variation in tropical trees: patterns of genetic
organization. New Forests 6, 67–94.
Lynch, M., Milligan, B.G., 1994. Analysis of population genetic structure with
RAPD markers. Mol. Ecol. 3, 1–9.
Navarro, C., 2002. Genetic resources of Cedrela odorata and their efficient use
in Mesoamerica. Academic Dissertation in Forest Tree Breeding. University
of Helsinki, Finland.
339
Nei, M., 1972. Genetic distance between populations. Am. Nat. 106, 283–292.
Nei, M., 1973. Analysis of gene diversity in subdivided populations. Proc. Natl.
Acad. Sci. 70, 3321–3323.
Novick, R., Dick, C., Lemes, M., Navarro, C., Caccone, A., Bermingham, E.,
2003. Genetic structure of Mesoamerican populations of big-leaf mahogany
(Swietenia macrophylla) inferred from microsatellite analysis. Mol. Ecol.
12, 2885–2893.
Patiño, F., 1997. Los Recursos Genéticos de Swietenia macrophylla y Cedrela
odorata en los neotrópicos: prioridades para una acción coordinada.
Recursos Genéticos Forestales 25, 21–33.
Pennington, T.D., Styles, B.T., 1975. A generic monograph of the Meliaceae.
Blumea 22, 419–540.
Rivera-Ocasio, E., Aide, T.M., McMillan, O., 2002. Patterns of genetic diversity
and biogeographical history of the tropical wetland tree, Pterocarpus
officinalis (Jacq.), in the Caribbean basin. Mol. Ecol. 11, 675–683.
Vekemans, X., Beauwens, T., Lemaire, M., Roldan-Ruiz, I., 2002. Data from
amplified length polymorphism (AFLP) markers show indication of size
homoplasy and a relationship between degree of homoplasy and fragment
size. Mol. Ecol. 11, 139–151.
Vos, P., Hogers, R., Bleeker, M., Reijans, M., Van de Lee, T., Hornes, M.,
Frijters, A., Pot, J., Peleman, J., Kuiper, M., Zabeau, M., 1995. AFLP: a new
technique for DNA fingerprinting. Nucleic Acids Res. 23, 4407–4414.
Wright, S., 1931. Evolution in Mendelian populations. Genetics 16, 97–
159.
Yeh, F.C., 2000. Population genetics. In: Young, A., Boshier, H., Boyle, T.
(Eds.), Forest Conservation Genetics. CABI publishing, Wallingford, England/CSIRO Publishing, Collingwood, Victoria, pp. 21–37.
Zhivotovsky, L., 1999. Estimating population structure in diploids with multilocus dominant DNA markers. Mol. Ecol. 8, 907–913.