Insights into phylogenetic divergence of Dalbergia (Leguminosae: Dalbergiae) from Mexico and Central America

Abstract

The pantropical genus Dalbergia includes more than 250 species. Phylogenetic studies of the group are scarce and have only included two or three species distributed in Mexico. We obtained herbarium samples of Mexican, Central American, and South American species (sourced from MEXU). In addition, sequences of GenBank accessions were used to complement the study. Using internal transcribed spacer (ITS), the matK and rbcL sequences from 384 accessions comprising species from America, Asia, and Africa were sampled to evaluate phylogenetic relationships of Mexican species and infrageneric classifications based on morphological data. Phylogenetic analyses suggest that the genus Dalbergia is monophyletic and originated in South America. The species distributed in Mexico are not a monophyletic clade but are divided into four clades with affinities to South American and Asian species clades. There is no correlation between geography and large-scale phylogeny. The estimated ages of the Mexican and Central American clades ranged from 11.32 Ma (Dalbergia granadillo clade) to 1.88 Ma (Dalbergia ecastaphyllum clade). Multiple long-distance dispersal events should be used to explain the current genus distribution.

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fevo-10-910250 July 23, 2022 Time: 15:51 # 1
TYPE Original Research
PUBLISHED 28 July 2022
DOI 10.3389/fevo.2022.910250
OPEN ACCESS
EDITED BY
Jonathan J. Fong,
Lingnan University, China
REVIEWED BY
Harald Schneider,
Xishuangbanna Tropical Botanical
Garden (CAS), China
Maria M. Romeiras,
University of Lisbon, Portugal
*CORRESPONDENCE
Solange Sotuyo
jssotuyo@ib.unam.mx
†These authors have contributed
equally to this work and share first
authorship
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RECEIVED 01 April 2022
ACCEPTED 28 June 2022
PUBLISHED 28 July 2022
CITATION
Sotuyo S, Pedraza-Ortega E,
Martínez-Salas E, Linares J and
Cabrera L (2022) Insights into
phylogenetic divergence of Dalbergia
(Leguminosae: Dalbergiae) from
Mexico and Central America.
Front. Ecol. Evol. 10:910250.
doi: 10.3389/fevo.2022.910250
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© 2022 Sotuyo, Pedraza-Ortega,
Martínez-Salas, Linares and Cabrera.
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not comply with these terms.
Insights into phylogenetic
divergence of Dalbergia
(Leguminosae: Dalbergiae) from
Mexico and Central America
Solange Sotuyo1*†, Euler Pedraza-Ortega1†,
Esteban Martínez-Salas1, José Linares2and Lidia Cabrera1
1Departamento de Botánica, Instituto de Biología, Universidad Nacional Autónoma de México,
Mexico City, Mexico, 2Centro Universitario Regional del Litoral Atlántico (CURLA), La Ceiba,
Honduras
The pantropical genus Dalbergia includes more than 250 species.
Phylogenetic studies of the group are scarce and have only included two
or three species distributed in Mexico. We obtained herbarium samples
of Mexican, Central American, and South American species (sourced from
MEXU). In addition, sequences of GenBank accessions were used to
complement the study. Using internal transcribed spacer (ITS), the matK
and rbcL sequences from 384 accessions comprising species from America,
Asia, and Africa were sampled to evaluate phylogenetic relationships of
Mexican species and infrageneric classifications based on morphological data.
Phylogenetic analyses suggest that the genus Dalbergia is monophyletic
and originated in South America. The species distributed in Mexico are not
a monophyletic clade but are divided into four clades with affinities to
South American and Asian species clades. There is no correlation between
geography and large-scale phylogeny. The estimated ages of the Mexican and
Central American clades ranged from 11.32 Ma (Dalbergia granadillo clade)
to 1.88 Ma (Dalbergia ecastaphyllum clade). Multiple long-distance dispersal
events should be used to explain the current genus distribution.
KEYWORDS
barcode, Dalbergia, diversification, Miocene, Mexico
Introduction
The subfamily Papilionoideae includes an important clade, the Dalbergiodeae group.
The “Dalbergioides” represent a monophyletic group comprising all genera referred to
as the tribes Adesmieae and Aeschynomeneae, the subtribe Bryinae of Desmodieae and
Dalbergieae except the genera Andira,Hymenolobium, Vatairea, and Vataireopsis (Lavin
et al.,2001). This group consists of the subclades Adesmia,Dalbergia, and Pterocarpus,
supported and identified mainly on a molecular data basis (chloroplast sequences; the
trnK/matK spacer and the trnL intron, Lavin et al.,2001).
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The Dalbergia genus is a pantropical group with around
250 species and centers of diversity in Central and South
America, Africa, Madagascar, and Asia (Klitgård and Lavin,
2005). In Mexico, Dalbergia comprises 20 species, of which six
are endemic (Sousa et al.,2001;Linares and Sousa,2007;Ricker
et al.,2013). Dalbergia, or rosewoods as are generally known,
distinguishes because their heartwood is considered of high
economic value, owing to its beauty, durability, and excellent
physical, mechanical, and acoustic properties (Pittier,1922).
They also produce metabolites, used as antimicrobial (Rutiaga-
Quiñones et al.,2010), antifungal (Rutiaga-Quiñones et al.,
1995;Barragán-Huerta et al.,2004), antibiotic, antioxidants,
and cytotoxic agents (Hamburger et al.,1987;Lianhe et al.,
2011;Pérez-Gutiérrez and García-Baez,2013). In addition, it
has been reported that Dalbergia species establish symbiotic
relationships with rhizobia for nitrogen fixation. This plays an
important role in ecosystems since it improves soil fertility
(Rasolomampianina et al.,2005). The species populations are at
risk because of its intensive use, habitat loss, and fragmentation
as well as slow recruitment rate and growth. Several species of
the genus are used as timber species, and they are intensively
exploited and subject to international traffic. Conservation of
timber species threatened by illegal logging and deforestation is
essential. Barcodes of the species could help to monitor species
of Dalbergia subject to international traffic and reconstruct a
phylogenetic hypothesis of the genus.
Phylogenetic analyses of the tribe Dalbergieae are based
on molecular and morphological data (Lavin et al.,2001),
placing Dalbergia in the Dalbergia clade as sister to the genus
Machaerium Pers. and Aeschynomene L. subgen. Ochopodium.
Later on, Ribeiro et al. (2007)concluded that Aeschynomene
subgen. Ochopodium Vogel is more closely related than
Machaerium to Dalbergia.Vatanparast et al. (2013)made
other attempts to resolve the generic relationships between
Aeschynomene and other segregate genera (Bryaspis,Geissaspis
Wight & Arn. and Kotschya Endl.), but they are weakly
resolved still. Cardoso et al. (2020), studying the phylogenetic
relationships of Aeschynomene subgen. Ochopodium, find
that both, Aeschynomene and Machaerium, are sister taxa of
Dalbergia. Ochopodium section was newly circumscribed as
Ctenodon, and the genus is particularly diverse in Mexico and
Brazil and has a few endemic species in the Andes.
In Mexico, 20 species have been described, 15 of which
are potentially threatened by illegal logging (Linares and
Sousa,2007). Due to the characteristics of its wood, they are
over-exploited, placing them in danger of extinction (NOM-
059 SEMARNAT,2010). According to the red list of the
IUCN (International Union for Conservation of Nature), the
species of the most concern are Dalbergia granadillo and D.
retusa, as their natural populations are decreasing considerably
and are therefore considered Critically Endangered (IUCN).
Mexican species inhabit the west and center of the country
and the Yucatan peninsula. However, most species grown in
the southeast are associated with tropical forests, cloud forests,
tropical deciduous and sub-deciduous forests, and pine-oak
forests (Standley,1922) (Table 1). Only three Mexican species
were used in previous phylogenetic studies.
Dalbergia species are morphologically variable and possess
a wide range of habitat preferences which made it difficult to
classify the New and Old World species into natural groups
(Bentham,1860;Prain,1904;Carvalho,1989). It is necessary
to use several specimens for each species in a broadscale
distribution to get a more clear idea of which are the taxonomic
circumscription within Dalbergia species. We employed a
relatively wide taxonomic sampling using several Dalbergia
accessions from species occurring in Mexico and included
species from its centers of diversity in America, Africa, and Asia.
The objectives of this study were to (1) provide a phylogenetic
framework for Mexican Dalbergia species, (2) test up barcode
molecular markers in Mexican species, and (3) provide an age of
divergence for the Mexican species.
Materials and methods
Taxa sampling and deoxyribonucleic
acid sequencing
To obtain an in-depth view of the phylogenetic relationships
within the genus, we increased the previous sampling by the
addition of Mexican, Central America, and South American
species of Dalbergia. We included a total of 287 Dalbergia
accessions. Outgroup selection was based on previous
phylogenetic studies ensuring that accession sequences
from Ctenodon,Machaerium, and Pictetia close relative genera
were represented (Supplementary Table 1). A summary of
accessions used for species from Mexico, Central America, and
the Caribbean is listed in Table 2.
The sample tissue material for DNA extraction was obtained
from specimens in the MEXU herbarium. Total genomic DNA
was extracted from leaves, flowers, or fruit samples using a
modified DNeasy Plant Mini Kit (Qiagen). The target DNA
regions, rbcL and matK, were amplified with universal barcoding
primers (CBOL Plant Working Group,2009). In the case of
internal transcribed spacer (ITS), AB101 and AB102 primers
(Sun et al.,1994) were used. PCR amplification of rbcL,matK,
and ITS was carried out on a Gene Amp 2700 (Applied
Biosystems, United States) with a Thermo PCR Master Mix
kit (Thermo Fisher), using the manufacturer’s instructions.
PCR conditions for matK and rbcL were as follows: 2 min
initial denaturation at 94◦C, 35 cycles (94◦C 1 min, 52◦C
1 min, and 72◦C 1 min), and 10 min of final extension at
72◦C. PCR conditions for ITS were as follows: 2 min initial
denaturation at 94◦C, 35 cycles (94◦C 1 min, 53◦C 1 min,
and 72◦C 1 min), and 7 min of final extension at 72◦C.
Amplified PCR products were checked on 1% agarose gel
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TABLE 1 Ecological and morphological information of Dalbergia species distributed in Mexico, Central America, and the Caribbean.
Species IUCN Habit Habitat Altitude
(m)
Leaflet
number
Flower size
(mm)
Ovary
indumentum
Fruit shape Fruit texture Fruit
dispersion
D. agudeloi NT tree oak forest, seasonal dry forest 750-200 (11−)13
(−15)
4-4.5 villose unknown unknown anemocory?
D. brownei LC Scandent shrub
or liana
coastal scrub, mangroves, flooded
forests
0-20 1 7-11 grabrous oblong-lunate woody Hydrocoric
D. calderonii CR tree tropical deciduous forest,
medium deciduous forests
400-1200 5-6 4-5 velutine oblong woody Anemocory
D. calycina VU tree Quercus forest, cloud forest (800−)
1000-1900
(5-)9(-11) 17-20 glabrous? oblong chartaceous Anemocory
D. chontalensis VU shrub seasonal dry forest, riparian
vegetation, coastal vegetation.
0-1000 11-15 10-12 glabrous? elliptic subchartaceous anemocory
D. congestiflora EN tree tropical deciduous forest 0-600 7-13 3-4 pubescent oblong papyraceous Anemocory
D. cubilquitzensis LC tree tropical evergreen forest 0-900 (11−) 13-15 5-6 pubescent elliptic-oblong papyraceous Anemocory
D. ecastaphyllum LC Scandent shrub
or liana
coastal scrub, mangroves, flooded
forests
0-20 1 8-9 glabrous? suborbicular woody hydrocoric
D. glabra LC Scandent shrub
or liana
seasonal dry forest, riparian
vegetation
0-800 (7−)9 7-11.5 glabrous/pubescent elliptic to oblong chartaceous hydrocoric?
D. glomerata CR tree tropical evergreen forest, tropical
oak forest
0-900 (5−) 9-11
(−12)
4.7-5.5 glabrous? elliptic-oblong chartaceous anemocory
D. granadillo CR tree tropical deciduous forest, oak
forest, rain forest
0-100 (13−) 11
(−15)
20 ? elliptic-oblong chartaceous anemocory
D. longepedunculata EN tree deciduous forest, evergreen forest 600-1100 7 (8−) 6 pubescent adaxially oblong chartaceous anemocory
D. luteola CR tree seasonal dry forest, riparian
vegetation in oak forest
800-1100 11-13 3-3.6 glabrous? unknown unknown anemocory
D. melanocardium EN tree montane rain forest 1300-1600 7-11 (−13) 5-6 villose oblong woody anemocory
D. monetaria LC S candent shrub
or liana
humid forests, mangroves 0-30 3–5 (–6) 5–6 glabrous? orbicular woody hydrocoric
D. palo-escrito EN tree cloud forest 1000-2000 9-13 3-5.5 puberulus oblong papyraceous anemocory
D. retusa CR tree dry seasonal forest, rain forest?,
gallery forest
20–1000 7–15 (−17) (8–) 15–18 (–20) glabrous? elliptic to oblong woody anemocory
D. stevensonii CR tree low deciduous forest 0-200 5 5-6 villose oblong woody anemocory
D. tabascana ? Scandent shrub
or liana
swamps, mangroves, lagoons,
savannahs and coastal vegetation
0-100 5-7 10-11.5 glabrous? oblong-lunate woody hydrocoric
D. tucurensis EN tree cloud forests, pine and pine-oak
forest
1400-2500 (11−) 13-15 4.5-6 densely villose oblong papyraceous anemocory
D. tilarana EN tree pine-oak forest, medium forests 600-1450 5-9 4-11 densely strigose elliptic to oblong woody anemocory
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TABLE 2 The phylogenetic clades recognized in the present study for
Mexican species of Dalbergia.
Clade Species N◦accessions sampled
Dalbergia ecastaphyllum D. monetaria 0
D. ecastaphyllum 3
Dalbergia glabra D. brownei 2
D. chontalensis 2
D. glabra 4
D. tabascana 2
Dalbergia glomerata D. agudeloi 2
D. calderoni 2
D. congestiflora 1
D. cubilquitzensis 7
D. glomerata 2
D. longepedunculata 2
D. luteola 3
D. melanocardium 4
D. palo-escrito 1
D. stevensonii 2
D. tucurensis 2
Dalbergia granadillo D. calycina 3
D. granadillo 3
D. retusa 5
electrophoresis. Both strands of the clean PCR products were
directly sequenced using BigDye Terminator v.3.1 (Thermo
Fisher, Foster City, CA, United States) cycle sequencing kit
and visualized on an ABI 3730 (Applied Biosystems) at
Laboratorio de Secuenciación Genomica de la Biodiversidad
y la Salud, Instituto de Biología, using the same primers as
for amplification.
Distribution maps
We constructed distribution maps with collection
information accessed from Global Biodiversity Information
Facility (GBIF.org,2022).1We downloaded 11,941 herbaria
records for Mexican, Central American, and Caribbean
species of Dalbergia sampled in the molecular phylogeny.
Data cleaning involved, first, standardizing data, deleting
duplicate specimens, deleting records without any geographical
coordinates, and any georeference erroneously georeferenced.
After that, we used the R package “CoordinateCleaner” (Zizka
et al.,2019) for further cleaning about coordinates at sea,
country and province centroids, country capitals, urban
areas, and around biodiversity institutions, which often come
from cultivated individuals or with incorrect data. From
the records downloaded, 5840 records were georeferenced,
and after filtering and cleaning, 4,014 records were suitable
to be used to generate distribution maps by species and
phylogenetic clade.
1www.gbif.org
Data analysis
Sequences were edited and assembled using SeqTrace
software (Stucky,2012). All sequences generated in this study
were deposited in GenBank (Supplementary Table 1). Edited
sequences for each gene region were aligned separately with
MAFFT (Katoh et al.,2009). After an initial alignment, the
alignments were manually adjusted using AliView (Larsson,
2014) if needed, following the principles described in Kelchner
and Clark (1997). In addition, we compiled all ITS, matK, and
rbcL sequences publicly available in GenBank for Dalbergia and
added our newly generated three loci sequences to that dataset
to produce a phylogenetic tree with a denser sampling across
Dalbergia. Sequences generated from the same voucher from at
least two loci have been used in the combined dataset to reduce
the missing data. The combined dataset has 194 accessions
and 336 accessions for the unique ITS dataset. A total of 384
accessions were analyzed.
Phylogenetic reconstruction of all the taxa sampled was
undertaken using Bayesian inference (BI). We used three
datasets: (1) the individual ITS dataset (unique ITS), (2) the
plastid data set, and (3) the concatenated dataset. A Bayesian
analysis without a molecular clock for the concatenated matrix
was inferred with MrBayes. Gene trees for calibration were
inferred with BEAST2 (Bouckaert et al.,2019). The GTR + 0was
selected as the best fit model based on the Akaike information
criterion (Akaike,1974) using the software jModelTest 2
(Darriba et al.,2012). The combined analysis for the three
markers was run in 20 ×106 generations, sampling every 1,000.
For the ITS dataset, 40 ×106 generations were run. Trees
were sampled for 1,000 generations, and 20% of them were
discarded as burn-in. The convergence of MCMC chain trees
was visualized with the Bestiary software (Wirth and Duchene,
2021). Calibrated time trees were estimated using BEAST2
(Bouckaert et al.,2019) with a Yule tree prior model, lognormal
relaxed molecular clock, and the node Machaerium-Dalbergia
data according to Lavin et al. (2005). The trees were visualized
with ggtree for R (Yu,2020). Alignments in FASTA format can
be seen in the Supplementary Material (S2).
Results
Phylogenetic relationships, combined
tree
Phylogenetic trees show that Dalbergia is monophyletic (1.0
PP) with a basal clade formed by South American Neotropical
species (Dalbergia miscolobium, Dalbergia spruceana, and
Dalbergia villosa, sect Dalbergia sensu Carvalho,1997) resolved
sister to the remaining species (Figures 1,2). The second
clade of Asian species, containing two subclades, is then sister
to the remaining species. Subclade II-A of Mexican climbing
or woody vine species part of Ecastaphyllum sensu Carvalho
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FIGURE 1
Bayesian combined phylogram of Dalbergia. Under the branches, posterior probabilities (pp) are in red font.
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FIGURE 2
Combined Bayesian calibrated tree of Dalbergia. Above the branches, the estimated age range of the clades is in black font. Local posterior
probabilities are shown under branches in red font. Shading bottom bars represent geological epochs. The diamond mark represents the
calibration node. The bars on the branches represent the range of the 95% confidence interval in the Bayesian tree.
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(1997)(Dalbergia ecastaphyllum, Dalbergia monetaria) is sister
to subclade II-B of woody vine Asian species: Dalbergia velutina,
Dalbergia pinnata (synonym of Dalbergia tamarindifolia), and
Dalbergia rubiginosa (series Polyphyllae, Rubiginosae, Sericeae,
and Velutina sensu Prain,1904).
Clade III contains three subclades (III-A, III-B, and III-
C). Subclade III-A contains Asian species Dalbergia ovata
(Ovatae), Dalbergia cochinchinensis, and Dalbergia latifolia
(serie Latifoliae), both parts of section Miscolobium. Subclade
III-B contains Mexican and Central American species: Dalbergia
calycina, D. granadillo, D. retusa, and Dalbergia cuscatlanica.
Subclade III-C contains Asian species, and the species are part of
subgenus Amerimmnon sensu Prain (1904)section Dalbergaria;
Dalbergia cana (Canae) is the sister species of Dalbergia oliveri
(Lanceolarieae); then, they are the sister group of Dalbergia
stipulacea (Stipulaceae)-Dalbergia volubilis (Volubilis), and
the group formed by seven species part of Lanceolarieae
(Dalbergia lanceolaria subsp. lanceolaria, Dalbergia balansae,
Dalbergia huapeana, Dalbergia assamica, Dalbergia nigrescens,
and Dalbergia paniculata) and Sericeae (Dalbergia sericea).
Clade IV is formed by five subclades (IV-A, IV-B,
IV-C, IV-D, and IV-E). Subclade IV-A is formed by the
tree species of Dalbergia latifolia (Latifoliae) and Dalbergia
melanoxylon (Phyllanthoides). Subclade IV-B is formed by
Dalbergia dyeriana, Dalbergia hancei (Foliaceae), Dalbergia
cultrata (Cultratae), and Dalbergia horrida. Subclade IV-C is
formed with four climbing Mexican–Central American species
(Dalbergia brownei, Dalbergia chontalensis, Dalbergia glabra,
and Dalbergia tabascana). Subclade IV-D includes a divergent
climbing species Dalbergia subcymosa (Ecastaphyllum sensu
Carvalho,1997) from South America as a sister to the following
Asian species: Dalbergia trichocarpa (Madagascar-African tree,
unknown sect.), the tree Dalbergia sissoo (serie Sisso), the woody
climbers Dalbergia rimosa (serie Rimosae), and Dalbergia
entadoides (unknown sect.-serie), and the tree Dalbergia
odorifera (unknown sect.-serie). Subclade IV-E resolves a group
of South American tree species of Triptolemea sensu Carvalho,
1997 (Dalbergia variabilis =Dalbergia frutescens, Dalbergia
cearensis, Dalbergia riparia, and Dalbergia brasiliensis) as the
sister group of 10 Mexican–Central American species of trees
(Dalbergia agudeloi, Dalbergia melanocardium, Dalbergia palo-
escrito, Dalbergia tucurensis, Dalbergia calderonii, Dalbergia
stevensonii, Dalbergia cubilquitzensis, Dalbergia glomerata,
Dalbergia longepedunculata, and D. calycina).
Phylogenetic relationships, internal
transcribed spacer tree
In this tree, we included a larger number of species
from Africa (Figure 3). Dalbergia is monophyletic with a
basal clade formed by South American Neotropical species
(D. miscolobium, D. spruceana, Dalbergia foliolosa, Dalbergia
cuiabensis, D. villosa, Dalbergia acuta, Dalbergia revoluta,
Dalbergia inundata, and Dalbergia lateriflora) resolved sister to
Dalbergia afzeliana from Africa. The second clade is formed by
two subclades: one of Mexican climbing or woody vine species
(D. ecastaphyllum and D. monetaria) as sister to a subclade
of woody vine Asian species (D. pinnata, D. tamarindifolia,
D. rubiginosa, Dalbergia candenatensis, Dalbergia rostrata, D.
stipulacea, and D. velutina) and an African bush species
(Dalbergia microphylla).
Clade III contains three subclades. The first contains
Asiatic species (Dalbergia ovata,D. cochinchinensis, Dalbergia
sissoides, and D. latifolia) and African tree species (Dalbergia
maritima, Dalbergia capuronii, and Dalbergia boehmi). The
second one is with Mexican and Central American species
(D. calycina, D. granadillo, and D. retusa). The last subclade
has a group of African species (Dalbergia lactea, Dalbergia
aurea, and Dalbergia bignonae) as sister of a clade with Asian
species grouped into three clades: the first one grouping
D. cana,D. oliveri, D. hancei, and Dalbergia lakhonensis;
second one grouping D. stipulacea,Dalbergia yunnanensis,
D. volubilis, D. paniculata, and D. nigrescens; and the
third one formed by D. sericea, D. lanceolaria, Dalbergia
godefroyi, D. stipulacea, Dalbergia huepeana, D. balansae, and
D. assamica.
Clade IV is formed by five subclades. The first subclade
is formed by a climber African species Dalbergia hostilis and
two Asian species (Dalbergia sandakanensis and Dalbergia
bintuluensis). In the second subclade, three climbing and one
small tree species from Mexico-Central America (D. brownei,
D. chontalensis, D. glabra, and D. tabascana) are nested with
D. nigra from Brazil; these species are the sisters of an
Asian group formed by D. dyeriana, D. hancei, D. cultrata,
Dalbergia thorelii, Dalbergia lunghuhnii, and D. horrida. The
third subclade has African species Dalbergia bracteolata and
D. boehmii as the sister group of a clade with the tree species
Dalbergia latifolia and D. melanoxylon. The fourth subclade
has Dalbergia canescens and Dalbergia benthamii from Asia,
South American species (D. cearensis, Dalbergia decipularis,
D. variabilis =D. frutescens, D. brasiliensis, D. riparia,
and Dalbergia frutenscens var. tomentosa), and 12 Mexican–
Central American species of trees (D. agudeloi, D. calderonii,
Dalbergia congestiflora, D. cubilquitzensis, D. glomerata, D.
longepedunculata, Dalbergia luteola, D. melanocardium, D. palo-
escrito, Dalbergia tilarana, D. tucurensis, and D. stevensonii).
The fifth subclade includes an African group of trees
(D. trichocarpa, Dalbergia greveana, Dalbergia abrahamii,
Dalbergia humbertii, Dalbergia bojeri, and Dalbergia baronii)
with two divergent climbing species (D. subcymosa from South
America and Dalbergia martii from Africa) as sister to Asian
species. This group of Asiatic species consists of a divergent
tree species (D. cultrata) sister to a subclade formed by woody
climbers (D. rimosa,Dalbergia cf. kingiana, and Dalbergia
dialoides), plus a tree species (D. sissoo), and a mix of trees,
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FIGURE 3
ITS calibrated tree of Dalbergia. Above the branches, the estimated age range of the clades is in black font. Local posterior probabilities are
shown under branches in red font. Shading bottom bars represent geological epochs. The diamond mark represents the calibration node. The
bars on the branches represent the range of the 95% confidence interval in the Bayesian tree.
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FIGURE 4
Tanglegram illustrating the discordance between the ITS gene tree (nrITS) and the combined plastid gene tree (cp) for Dalbergia. Links connect
identical tips, with nodes rotated to minimize link overlap. Links are colored by geographical distribution. Clades that are similar between the
two trees are indicated by black circles with white font. Tipuana tipu was eliminated because only the ITS1 sequence was available.
lianas, and woody climbers (D. odorifera, Dalbergia tonkinensis,
D. yunnanensis, Dalbergia rimosa var. foliacea, D. entadoides,
and Dalbergia parviflora).
There are not many obvious relationships conflicting
between the nuclear loci tree and the two loci concatenated
plastid tree (Figure 4). The backbone of the plastid loci tree is
nearly identical to the nuclear ITS tree, with all major nodes
and monophyly receiving strong support. In the plastid tree,
there are many polytomies but a geographical structuring of the
species is observed. The major clades disappear hierarchically
but still form a group. The major conflict in the tanglegram is
Dalbergia melanoxylum, in ITS tree is a sister species to D. glabra
clade, and in plastid tree is part of a polytomy.
Geographical distribution of Mexican,
Central American, and Caribbean
species of Dalbergia
Most tree species of Dalbergia are restricted in distribution
with the exception of D. congestiflora. Populations of
D. granadillo clade are mostly distributed along the Pacific
coast of Mexico from Colima to Panama. Climbing species
have more widespread distributions, like D. ecastaphyllum and
D. monetaria whose distribution reaches South America and
Africa. D. brownei is a climbing species that has managed to
spread as far as the coast of Florida. Distribution maps by clade
can be found in Figure 5. Distribution maps by species can be
found in Figures 1–5 of the Supplementary Material.
Divergence time estimates
Divergence time estimation provided a robust time-
calibrated tree of Dalbergia (Figure 2). The Dalbergia group
arose 34.42 Ma during the Oligocene and diversification of
the present day occurred during the Miocene to Pleistocene
from 34.42 to 1.88 Ma. Dalbergia diverged from their sister
genera 44.95 Ma and diversified during the Miocene (24.73–
5.23 Ma). The divergence ages for Mexican Dalbergia species
are between Quaternary (Pleistocene) and Tertiary (Neogene).
The oldest Mexican clade is Dalbergia granadillo with 11.32 Ma
(Miocene), D. congestiflora clade with 9.2 Ma (Miocene,
Tortonian), D. glabra with 6.63 Ma (Miocene, Zancleane),
and D. ecastaphyllum with 1.88 Ma (Pleistocene, Calabrian).
Divergence estimations from the combined tree to the ITS tree
do not vary considerably (Figure 3). The estimation age for
the Dalbergia granadillo clade was 11.5 Ma, for D. glomerata
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FIGURE 5
Distribution maps by clade for Dalbergia species from Mexico, Central America, and the Caribbean.
clade was 9.7 Ma, for D. glabra clade was 6.7 Ma, and for
D. ecastaphyllum clade was 2.2 Ma.
Discussion
Taxonomy
Bentham (1860)divided the 64 species of Dalbergia
known into six series (Triptolemea Americanae, Triptolemea,
Sissoae Americanae, Sissoae Gerontogee, Dalbergariae, and
Selenolobium). von Taubert (1894)divided the species into four
sections (Triptolemaea, Sissoa, Dalbergaria, and Selenolobium).
In the Neotropics, the 44 Brazilian species of Dalbergia were
divided into five sections by Carvalho (1989,1997)based
on inflorescence and fruit types (Dalbergia, Ecastaphyllum,
Pseudoecastaphyllum, Selenobium, and Triptolemea). In
Asia, Prain (1904)classified the 86 South-East Asian species
of Dalbergia into two subgenera (Amerimnon and Sissoa),
five sections (Dalbergaria, Endespermum, Miscolobium,
Podiopetalum, and Triptolemea) and 24 series. Finally,
Thothathri (1987)categorized the 46 Dalbergia species, present
in the Indian subcontinent, into four sections and seven series
based on androecium and fruit types.
The sect. Triptolemea, with cymose inflorescences and
samaroid legume, and sect. Ecastaphyllum, with racemose or
paniculate inflorescences and orbicular to reniform legume
sensu Carvalho (1997), are monophyletic. These sister
relationships between species have also been found by Ribeiro
et al. (2007);Vatanparast et al. (2013), and Hartvig et al.
(2015). We also found relationships between D. candenatensis,
D. pinnata, and D. velutina as other authors do (Vatanparast
et al.,2013;Hartvig et al.,2015) but no as sister species.
They are part of the same clade with D. tamarindifolia (sister
to D. pinnata), D. rubiginosa, and D. sericea.Niyomdham
et al. (1997)recognized that D. pinnata, D. candenatensis,
and D. velutina have morphological affinities in the lower
calyx tooth as long as or slightly longer than the laterals,
standard equal to at least 3/4 of the blade, sometimes exceeding
it. Niyomdham et al. (1997)treated D. tamarindifolia as a
synonym of D. pinnata, specimens occurring together into
the clade in two groups; these results might be indicative of
taxonomic differences.
We found that sect. Dalbergia sensu Carvalho (1997)is
also monophyletic. Species sampled from section Dalbergiaria
sensu Prain (1904)are monophyletic too (series Lanceolarieae,
Stipulaceae, and Volubilis). Vatanparast et al. (2013)treated
Dalbergia balansae and D. assamica as separate species, but
Hartvig et al. (2015)treated both species as a synonym. In
this study, we treated the species separately and we included
Dalbergia hupeana. Specimens in the phylogenetic analyses
occur together; D. hupeana and D. balansae are sister species
of D. assamica, as well as D. sericea, D. nigrescens, and
D. paniculata. These results might be indicative that D. balansae
and D. assamica are different species.
The Latifoliae series (D. latifolia, D. cochinchinensis,
and D. ovata) from section Miscolobium (Prain,1904) is
monophyletic, and this group was also found by Vatanparast
et al. (2013)and Hartvig et al. (2015). Morphological characters
between D. cochinchinensis and D. ovata are lower calyx teeth as
long or slightly longer than the lateral ones; standard longer than
wide; leaves with (5−) 7-9 leaflets; leaflets acute to acuminate,
apiculate, rarely obtuse, or rounded; flowers white to whitish,
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5.5–6 mm long; fruits thin, papyraceous, glabrous, light brown
(Niyomdham et al.,1997).
Accessions of Dalbergia rimosa are in three different groups
in the same subclade. The first group is the sister species
to D. odorifera, the second one is sister to D. entadoides,
and the third one is basal D. rimosa accessions. The species
is distributed in India, Myanmar, South of China, Thailand,
Laos, and Vietnam from 200 to 1,300 m in mixed deciduous
forests and scrub forests. When we see herbarium specimens
from the different country distributions, it is clear that
a morphological taxonomic revision must be carried out
(e.g., Hooker J.D. sn. from Myanmar, Berhaman et al. SAN
134566 from Malaysia).
Mexican, Central American, and
Caribbean species of Dalbergia
Although there is a taxonomic treatment for Flora
Mesoamericana (Linares,in press), since Pittier (1922)there
have been no attempts at subgeneric-level classifications of
Mexican Dalbergia.Richter et al. (1996), citing personal
comments by Richter et al. (1996), suggested four groups for
the Mexican species. The first consists of D. retusa,Dalbergia
hypoleuca,D. granadillo, and Dalbergia lineata, probably
D. cuscatlanica and Dalbergia pacifica, all of which are similar
in wood structure and metabolites.
The second group comprises Central American and
Mexican species, D. tucurensis (including D. cubilquitzensis),
D. palo-escrito,D. melanocardium,D. glomerata, D.
congestiflora, D. calderonii (including Dalbergia funera),
and probably D. stevensoni. No differentiation was detected
in the wood of these species, although Richter et al. (1996)
underline that D. stevensonii may be different from the rest.
The third group, with the species D. calycina and Dalbergia
intibucana (nowadays synonyms), were not sampled for
Richter’s study because of their lack of commercial value at that
time. Finally, the fourth group with D. brownei whose wood
parenchyma banding is similar to that found in D. congestiflora
and D. funera but different in the uniseriate rays.
Three of the groups hypothesized by Rudd are
phylogenetically valid. The first is referred to here as the
Dalbergia granadillo clade (because it is the most traded
species in the clade). Currently, only the following species
are recognized by Linares (in press),Dalbergia granadillo,
D. retusa var. retusa, and D. retusa var. cuscatlanica. To the
same clade belongs D. calycina which Rudd recognized as
a separate group and which is within the clade as the most
divergent species. The species are distributed in the seasonally
dry forests of the Pacific Coast of Mexico from Jalisco to Oaxaca
(D. granadillo), in the seasonally dry forests of Southeastern
Honduras, Nicaragua, and Costa Rica (D. retusa var. retusa),
and in humid environments of Honduras and El Salvador
(D. retusa var. cuscatlanica).
The second group is what we called the Dalbergia glomerata
clade. The D. glomerata clade is a group of 12 species distributed
in the Pacific Coast of Mexico from Jalisco to Costa Rica, in the
Rio Balsas Depression, in the Gulf Coastal plain from Veracruz
to North of Chiapas, and in Guatemala and Belize. Species
can be found in cloud forests, seasonally dry tropical forests,
tropical rainforests, or secondary vegetation. Sister species clade
is from South America (D. brasiliensis, D. riparia, D. cearensis,
and D. variabilis (D. frutescens)). They are part of Triptolemea
and characterized by inflorescence cymose in terminal racemes;
fruit oblong to elliptical, samaroid, with reticulate venation
more prominent over the seed cavity. Species occur mainly
in central and eastern Brazil, with the exception of D. riparia
that inhabits the central Amazon Basin and less frequently on
the lower Amazon.
Finally, the third group, referred to here as the Dalbergia
glabra clade (fourth group for Rudd), includes the species
D. brownei,D. chontalensis,D. glabra, and D. tabascana.
Rudd does not include the last three species, although, in
1995, she described varieties within D. glabra. The D. glabra
clade species are distributed from Veracruz, Mexico, to
Honduras on the Atlantic and from Oaxaca, Mexico, to
El Salvador in the Pacific Coast. Furthermore, Rudd did
not say anything about the species D. ecastaphyllum and
D. monetaria (D. ecastaphyllum clade). The D. ecastaphyllum
clade is distributed from Florida, United States, to Brazil,
passing through Mexico, and in Caribbean islands. Plant
distribution records exist in the Western part of Africa. Species
inhabits riparian vegetation, coastal dunes, mangrove forests,
and mangrove-associated forests.
Time of diversification in Dalbergia
The origin of Dalbergia is probably South America, as the
South American species are the earliest divergent. Later, the
genus must have migrated to North America (possibly when
Central America did not yet exist) and diversified into the
four lineages we recognize today. In Figure 6 (Supplementary
Material), we can see that all haplotypes are central (in green).
The Asian species evolved from the North American ones.
There are different lineages between them, probably during
the boreotropic (the only issue is that the geological data date
this stage in the Eocene, implying that the genus is possibly
older), which is in agreement with the fossil record found in
America and Europe. The South American lineage of Dalbergia
frutescens is a more recent arrival and derives from a southern
migration of the Dalbergia glomerata clade (Figure 1 and
Supplementary Material).
The Dalbergia granadillo clade must have had an ancestor
in mountain areas, tolerant of metamorphic rocky soils and dry
conditions, and equivalent to mixed pine-oak forest. The earliest
diverged species is D. calycina, a species found in montane areas
such as Bochil or in the Cañon del Sumidero, both in Chiapas.
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The Dalbergia glomerata clade can be divided into two
groups: (1) species related to D. cubilquitzensis (species
complex) that inhabit humid environments and are tolerant
of limestone and metamorphic soils, and (2) species
related to D. congestiflora that inhabit areas with marked
seasonality and dryness. Dalbergia stevensonii, which is
the most recently diversified species in the clade, has a
morphology that resembles species from the seasonal dry
forest and not from the humid and flooded area where it is
currently distributed.
The Dalbergia glabra clade mostly consists of climbing
species. The earliest divergent species, D. chontalensis, is a
shrub distributed in floodplains or near low-lying streams.
D. brownei is a shrubby, climbing species distributed on
coastal dunes and has dispersed as far as Florida. Dalbergia
tabascana is another lianoid species that has “specialized” to
grow in freshwater swamp areas. The area where it is currently
distributed was once a wetland area (San Lorenzo Tenochtitlán).
The most recently diversified species (Pleistocene) is D. glabra,
the only species in the clade that succeeded in diversifying
from seasonal dry forest environments associated with water
bodies to rain forests. Populations of this species can be
found in the interior of the country but are always associated
with water bodies.
The Dalbergia ecastaphyllum clade is the most recent
in origin, and the species that comprise it are two lianoid
species that inhabit mostly coastal regions. D. monetaria is the
most recent species, is tolerant of freshwater bodies, and can
therefore be found in different areas of the Amazon and in
the African Congo. The fruit is floating and woody and has a
“spongy” endocarp.
Most of the ages obtained here are younger than previous
estimates (Lavin et al.,2005). Lavin et al. (2005)using a matK
phylogenetic reconstruction estimated the age of divergence
between Dalbergia sisso and Tipuana tipu in 49.1 ±0.8 Ma
(47.1–51.4 Ma). In the same study, they estimated the
age of divergence between D. sissoo and Ormocarpum in
45.6 ±0.8 Ma (43.9–47.3 Ma). However, in the study of
Lavin et al. (2004), the reported Dalbergia estimation age
from stem and crown clades is 40.4–43.3 Ma, and they give
divergence estimates ranging from 12.7-3.8 to 7-12.2 Ma. Later
on, Hung et al. (2020)with transcriptomes data (256 single-
copy orthologs, 479,064 bp) established that the Dalbergia
miscolobium clade is basal with an age of ±14.78 Ma (Miocene-
Langhian). The divergence ages found for D. cochinchinensis
and D. oliveri in Indochina were estimated to be 11.68 Ma
(Lower Miocene), which corresponds with the separation
of the Thai–Malay Peninsula from Borneo ±15 Ma ago
(Vatanparast et al.,2013). The fossils of Dalbergia found in
Europe are from the Miocene such as Dalbergia nostratum
(15.97–23.03 Ma; lower Miocene), Dalbergia lucida (5.33–
11.61 Ma; late Miocene), or Dalbergia phleboptera (27.82–
23.2 Ma; Oligocene–Miocene). For Mexico, fossils of wood from
Puebla are dated from the Oligocene (32 Ma, Sainz-Reséndiz,
2011).
Miocene diversification of Dalbergia reflects patterns shown
in other tropical genera (Choo et al.,2020;Schley et al.,2022)
in accordance with the climatic and ecological changes that
occurred in the Tropics during the Miocene.
The combined marker phylogenetic reconstruction
indicated that in Mexico, several ancestral independent
lineages within Dalbergia might began their diversification
consecutively during the Miocene. The ancestors of Mexican
Dalbergia clades came from South America and Asia. How
species were exchanged from South America to Mexico can
be explained by migrations through Central America via the
narrow Isthmus of Panama, which existed above sea level from
the late Eocene to the Oligocene (38–28 Mya, Montes et al.,
2012), and through which the exchanges of flora and fauna
may have taken place (Cody et al.,2010). In the warm periods
from the Eocene to Miocene through the transport of seeds and
after the consolidation of the Isthmus, the contributions of flora
must have increased.
For the Dalbergia glomerata clade, the sister group of taxa
D. brasiliensis, D. cearensis, and D. variabilis (D. frutescens) have
a fruit that could be wind-dispersed, while D. riparia has a fruit
that is dispersed by water. The ancestor of the D. glomerata
clade could have been wind-dispersed through Panama Isthmus.
Physiographic conditions in Mexico at that time must have
facilitated the introduction of coastal and low-elevation species
through efficient mechanisms of long-distance seed dispersal
(e.g., ancestors of Dalbergia glomerata and D. granadillo). These
species then evolved in the Sierra Madre del Sur, which was still
active during the early Miocene, and, later on, in some areas
during the Pleistocene (Ferrari et al.,2005;Moran-Zenteno
et al.,2007). Likewise, the complex Trans-Mexican Volcanic
Belt generated hundreds of scenarios in Central Mexico from
the Miocene to the present (Ferrari et al.,2012) promoting
population divergence, and thus speciation.
Ancestors from Asia and Africa must have arrived in
America due to long-distance dispersal. How did they arrive
could have been by different routes. One of these ways could
have been by ocean currents. The tropical Atlantic belts where
surface currents and winds are simultaneously favorable for
East-West crossing are found between the Congo delta and the
Maranhão in Brazil and just North of the Senegal river delta and
Northern Brazil and the Guianas. Both streams originate in river
deltas in Africa. Parrish (1993)has suggested “rafting” transport
of organisms between South America and Africa during the
Tertiary and was probably predominantly from East to West
rather than the other way around (Renner,2004). Although
these currents may have been different during the warm climates
of the Eocene–Miocene, there is no evidence that they were
different from those of today. The only current that may have
been different is the one in the vicinity of the Isthmus of
Panama, before it closed. There are also data that the Rio Grande
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rise (Southeastern of the coast in Brazil) and the western end
of the Walvis Ridge (Southwest African Coast, Cape Town)
may have been above water until the Oligocene (Parrish,1993;
Morley,2000), reducing the distance between continental coasts.
Another form of long-distance dispersal using ocean currents
may have been by fruit flotation. Currently, we have a clear
example with Dalbergia ecastaphyllum and D. monetaria found
in America but also in the western portion of Africa and whose
fruits are frequent buoyants in marshes and rivers and can
remain floating up to nine months (Gunn et al.,1976). There
are Dalbergia species reported in the literature as Dalbergia
monosperma that are waterborne (Ridley,1990). Some of the
Asian species of Dalbergia have fruits with similar characteristics
to D. ecastaphyllum and D. monetaria to be transported, because
they have coriaceous to woody fruits with a single seed which
would form an air chamber inside, allowing them to float
(e.g., Dalbergia albertesii, Dalbergia beccarii, D. horrida, and
D. tamarindifolia).
Other options for long-distance transport are migratory
birds, but except for some Psittacidae that consume Dalbergia
seeds, there are no migratory species that could transport them
from Asia to America or vice versa. While only ocean currents
are heard as consistent for Dalbergia to be dispersed over
long distances, all of the above mechanisms together could
shape the diversity encountered in the genus today. Species
distribution must also be related to soil type and microbiome.
Rasolomampianina et al. (2005)found 68 strains of fixative
bacteria in eight endemic Dalbergia species from Madagascar.
Some of these strains such as Bradhirhizobium are common in
tropical legumes, but the others are specific.
Concluding remarks
The reconstructed evolutionary history of Dalbergia from
Mexico and Central America provides insights on how the
number of species present in the area may have originated.
Regarding genetic barcodes, the most commonly used for
Dalbergia have been ITS, matK, and rbcL, either alone or in
different combinations (Bhagwat et al.,2015;Hassold,2015;
Li et al.,2017). Li et al. (2017)recommend the combination
ITS +matK +rbcL to identify Dalbergia species. Our results
show that, for species from Mexico, Central America, and
the Caribbean, the ITS region is acceptable to distinguish
at the species level, and in combination with chloroplast
markers, we can know the area of provenance. Hassold
(2015), in her study with chloroplast markers, indicates that
plastid sequences reflect the geographical range and shared
haplotypes between species. The data obtained in this study
demonstrate that the whole piece of ITS alone can help
us to differentiate between Dalbergia species. If the area
of provenance is also required, it will be necessary to use
chloroplast sequences.
Data availability statement
The datasets presented in this study can be found in
online repositories. The names of the repository/repositories
and accession number(s) can be found in the
article/Supplementary Material.
Author contributions
SS designed the study, collected the materials, conducted the
experiments, drafted the manuscript, and secured funding for
the project. EP-O conceived and conducted the bioinformatic
analyses, reviewed the manuscript, and assisted in the
discussions. EM-S assisted in the discussions and reviewed
the manuscript. JL provided taxonomic advice, reviewed the
manuscript, and assisted in the discussions. LC trained students
in the laboratory and performed a first draft assembly of
sequences generated by this study. All authors contributed to the
article and approved the submitted version.
Funding
This study was supported by a grant from PAPIIT project
IA2015 to SS and operative funding to SS from Instituto
de Biología.
Acknowledgments
We thank Berenice Mendoza, Mayra Castillo, and José
Antonio Contreras-Chijate for their help in the laboratory. Our
special gratitude goes to Laura Márquez and Nelly López-Ortiz
for sequencing.
Conflict of interest
The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the
authors and do not necessarily represent those of their affiliated
organizations, or those of the publisher, the editors and the
reviewers. Any product that may be evaluated in this article, or
claim that may be made by its manufacturer, is not guaranteed
or endorsed by the publisher.
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Supplementary material
The Supplementary Material for this article can be
found online at: https://www.frontiersin.org/articles/10.3389/
fevo.2022.910250/full#supplementary-material
SUPPLEMENTARY FIGURES 1–5
Distribution maps by species.
SUPPLEMENTARY FIGURE 6
Haplotype network for plastid markers of Dalbergia.
SUPPLEMENTARY TABLE 1
List of Dalbergia species and allies used in this study.
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