ANALYSIS OF GENERIC RELATIONSHIPS
IN ANACARDIACEAE
B.S. WANNAN
Environmental Protection Agency, P.O. Box 802, Atherton 4883, Queensland, Australia
SUMMARY
Cladistic analyses were undertaken of Anacardiaceae using non-sequence data (30 genera and 81
characters from morphology, anatomy, palynology and chemotaxonomy), sequence data (26 genera
– rbcL) and a combined dataset of 16 genera. All analyses supported a group of genera which can be
recognised at the subfamily level: Anacardioideae. Sequence data and combined datasets supported
the recognition of a second subfamily: Spondiadioideae Kunth emend. Wannan. Both datasets also
suggested that Buchanania lies outside both subfamily groups.
Key words: Anacardiaceae, cladistics, phylogeny, rbcL sequence data.
INTRODUCTION
The Anacardiaceae is a well recognised world-wide family of mostly tropical trees
which has historically been placed in the Sapindales or Rutales (Bentham & Hooker,
1862; Takhtajan, 1980; Dahlgren 1980, 1983, 1989; Cronquist, 1981; Angiosperm Phylo-
geny Group, 1998; Judd et al., 1999). Cronquist (1981) placed it with the Julianiaceae
and Burseraceae, the three being the only families in the Sapindales with biflavonyls
and vertical intercellular secretory canals in the primary and secondary phloem. The
close relationships of the Anacardiaceae and Burseraceae have been recently reiter-
ated by analysis of rbcL and atpB sequence data (Gadek et al., 1996; Savolainen et al.,
2000a). The Burseraceae are distinguished by having two epitropous ovules per locule,
in contrast to the one apotropous ovule in the Anacardiaceae. The Burseraceae also fre-
quently possess lobed cotyledons in contrast to entire cotyledons in the Anacardiaceae.
Amphipterygium and Orthopterygium, once a separate family (Julianiaceae), are now
considered part of the Anacardiaceae based on molecular and non-molecular data
(Peterson & Fairbrothers, 1983; Wannan & Quinn, 1988, 1990, 1991; Angiosperm
Phylogeny Group, 1998; Judd et al., 1999, Savolainen et al., 2000b).
The Anacardiaceae is generally considered to constitute about 70 genera and 600 species
which are concentrated in the tropics of Africa, Asia and America with a smaller number
of species occurring in subtropical and temperate areas. A number of infrafamilial
classifications have been proposed in the Anacardiaceae (Bentham & Hooker, 1862;
Marchand, 1869, 1874; Engler, 1883, 1892), but the most widely used for the last 100
years has been the five tribes of Engler (1883, 1892, 1897) which are based on floral
characters and leaf dissection. A recent division of the family into five subfamilies by
Takhtajan (1987) appears not to have been well accepted.
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Published on 10 May 2006 http://dx.doi.org/10.3767/000651906X622427
© 2006 Nationaal Herbarium Nederland, Leiden University branch
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A range of systematic studies have tested the applicability of Engler’s tribal classifi
cation, the most comprehensive having used stem anatomy (Jadin, 1894) or wood
anatomy (Heimsch, 1942; Dadswell & Ingle, 1948; Kryn, 1953). These found support,
with some reservations, for Engler’s tribes. Young (1976) looked at the wood flavonoids
of 16 genera of the Anacardiaceae (including Julianiaceae), in the tribes Anacardieae,
Rhoeae and Spondiadeae, as well as representatives of the Burseraceae, Rutaceae,
Simaroubaceae, Cneoraceae, Meliaceae, Sapindaceae, Aceraceae, Hippocastanaceae
and Juglandaceae. He found that there was a range of 5-deoxyflavonoids which was
restricted to the Anacardiaceae (including Julianiaceae), but there were no clear pat-
terns at a tribal level.
More recently, Wannan & Quinn (1990, 1991) described the pericarp and floral morphol-
ogy in 30 genera sampling all tribes in the family. They found that the distribution of
reproductive, vegetative and secondary product character states did not closely reflect
the subfamily taxonomies of either Engler (1883, 1892) or Takhtajan (1987). Rather,
they found support for two informal groups, but suggested that these required further
study to confirm their status. The first (Group A) included Engler’s tribes Anacardieae
(without Buchanania), Rhoeae (without Pentaspadon and Campnosperma), Dobineeae
and Semecarpeae, and the second (Group B) included the Spondiadeae but with the
addition of Buchanania, Pentaspadon and Campnosperma. Work by Von Teichman and
associates has confirmed the importance of pericarp structure for illucidating generic
affinities in the family (Von Teichman & Robbertse, 1986a, b; Von Teichman, 1987,
1990, 1991, 1992, 1993; Von Teichman & Van Wyck, 1988, 1994). Recent studies of
seed anatomy (Pienaar & Von Teichman, 1998) and wood anatomy (Dong & Baas,
1993) have also provided support for Wannan & Quinn’s (1991) groups.
Support for Wannan & Quinn’s (1991) two informal groups has also been provided by
an unpublished analysis of anatomical, morphological and rbcL sequence data across
17 genera (Terrazas & Chase, 1996). Their conference abstract reported two clades,
broadly corresponding to Wannan & Quinn’s groups. Some of their sequence data were
included in a molecular analysis of the Sapindales (Gadek et al., 1996) which used
7 genera from the Anacardiaceae and three from the Burseraceae. This analysis showed
the Anacardiaceae and Burseraceae as sister groups, and two main clades in the Anacar-
diaceae corresponding to Group A and B but with Buchanania diverging prior to both.
Other sequence data (rbcL: Chayamarit, 1997) from an analysis of 16 Thai genera has
also provided some support for the informal groups of Wannan & Quinn (1991), but
the absence of bootstrap or decay analysis made it impossible to assess the strength
of support for their clades. Recent sequence data from the internal transcribed spacer
region from the ribosomal DNA has provided an indication of relationships amongst
genera referred to Engler’s Rhoeae or Wannan & Quinn’s (1991) subgroup A2 (ITS:
Miller et al., 2001). American species of Rhus s.s. (subgenera: Lobadium and Rhus)
were shown to be closely related and more distant from other genera of the Rhoeae
including Actinocheita, Cotinus, Malosma, Schinus, Searsia and Toxicodendron.
The relationships of some genera of the Rhoeae were also investigated by Aguilar-
Ortigoza et al. (2004) using non-sequence data. Their main focus was on the 6 species
of Pseudosmodingium from Mexico which were shown to be most closely related to
Bonetiella, also from Mexico. However, the larger clade, corresponding to genera of
B. S. Wannan: Analysis of generic relationships in Anacardiaceae
167
the Rhoeae, included Smodingium (Africa) and Mexican representatives of Cardena-
siodendron, Cotinus, Rhus and Toxicodendron. A subsequent paper by a similar team
(Aguilar-Ortigoza & Sosa, 2004) combined sequence (rbcL) and non-sequence data for
22 genera of Anacardiaceae. Both separate datasets show good support for Wannan &
Quinn’s Group A (18 genera, including Anacardium and Mangifera from Engler’s tribe
Anacardieae) but less support for Group B (3 genera). In both analyses Buchanania is
placed as a sister taxon to genera in Group A, but outside the clade with Group B genera.
Interestingly, the paper compares the Anacardiaceae clade with a clade of hemipteran
insects (Calophya spp.) which feed on the family; the later shows closely related spe-
cies feeding on Spondias and Buchanania. A conference abstract (Pell & Urbatsch,
2001) describing analyses of sequence data from the chloroplast genome (matK, trnL
and the intergenic spacer between the trnL exon and trnF) has strongly supported the
two groups of Wannan & Quinn (1991). Pell & Urbatsch (2001) reported two major
clades in the family: one with members of the tribes Rhoeae, Semecarpeae, Dobineeae
and Anacardieae, and the other with members of the Spondiadeae and a few members
of the Rhoeae. They also reported that the Anacardiaceae proved to be monophyletic.
Thus, there are some data which support the proposed infrageneric classification of
Wannan & Quinn (1991). As yet, however, there has not been any broad analysis of
generic relationships using the range characters which are known for the family. This
paper analyses the available morphological, anatomical, chemotaxonomical, cytologi-
cal, palynological characters and the available sequence data (rbcL) and aims to test
support for the two informal subfamily groups proposed by Wannan & Quinn (1991)
and identify key data gaps in the family.
METHODS
Non-sequence data
The terminal taxa used in this analysis are genera (Table 1) with characters scored
from usually more than one species. The characters used are listed in Table 2 and Ta-
ble 3a, b is the data matrix. A list of the autapomorphies is provided in Table 4. Many
descriptions of character states were reviewed for each taxon. In a few cases where
differing character states were argued in the literature, these were scored as multiple
states with each source cited. In most cases, however, a single reliable authority has
been cited in Table 3a, b following a critical analysis of the literature. Some unpublished
data are included and are supported by vouchers in Appendices A and B.
Sequence data
Sequences for the chloroplast encoded rbcL gene were obtained for a subset of taxa
either from GenBank or from the sources cited in Table 5. Sequences were aligned in
PAUP* (Version 4.0b10; Swofford, 2002).
Analyses
Heuristic parsimony analyses were performed in PAUP* set for tree bisection
reconnection branch swapping on the best trees. Multistate characters were treated
as polymorphisms. Multiple replicates of random taxon addition were employed to
search for multiple islands of trees, and the CONDENSE option was employed to delete
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duplicate trees. Support for clades was inferred using the bootstrap option in PAUP*
(Felsenstein, 1985) with 500 replicates, and also by decay values (Bremer, 1988;
Donoghue et al., 1992). Decay command files were created in MacClade version 4.05
(Maddison & Maddison, 2002) and executed in PAUP* using 10 replicates of random
taxon addition on each constraint tree. Output trees from PAUP* were transferred to
MacClade and manipulated to test other topologies and explore character state evolution.
Taxon No. of Natural distribution Subfamily Group
species
Trib
e
1
Group
2
ANACARDIACEAE
Amphipterygium 4 Mexico Unplaced
3
A
Anacardium 11 Tropical America Anacardieae A
Astronium 13 Tropical America Rhoeae A
Blepharocarya 2 Australia Rhoeae A
Buchanania 25 AsiaPacific, Australia Anacardieae B
Campnosperma 10 Tropical America, Madagascar, Rhoeae B
Seychelles, S.E. Asia, Malesia
Cotinus 4 Temperate northern hemisphere Rhoeae A
Cyrtocarpa 4 Tropical America Spondiadeae B
Dobinea 2 Himalaya, China Dobineeae A
Dracontomelon 8 China, Malesia, Pacific Spondiadeae B
Euroschinus 6 New Caledonia, Papua New Guinea, Rhoeae A
Australia
Harpephyllum 1 Southern Africa Spondiadeae B
Lannea 40 Africa, Arabia, Tropical Asia Spondiadeae B
Lithraea 4 South America Rhoeae A
Loxopterygium 4 South America Rhoeae A
Mangifera 35 Tropical Asia, Malesia Anacardieae A
Pentaspadon 6 Tropical Asia, Malesia, Pacific Rhoeae B
Pistacia 14 Eurasia, Malesia, Mexico, Africa Rhoeae A
Pleiogynium 2 Malesia, Pacific, Australia Spondiadeae B
Rhodosphaera 1 Australia Rhoeae A
Schinopsis 8 South America Rhoeae A
Schinus 27 South America Rhoeae A
Semecarpus 60 Indo-Malesia, Australia Semecarpeae A
Spondia
s
4
8 Tropical America, Asia
4
Spondiadeae B
Swintonia 12 Burma, Malesia Anacardieae A
Tapirira 15 Tropical America Spondiadeae B
Toxicodendron 30 America, Indo-Malesia Rhoeae A
BURSERACEAE
Bursera c. 100 Tropical America Burserea
e
5
Canarium c. 100 Africa, Malesia, Pacific, Australia Canariea
e
5
Garuga 4 Asia, Malesia, Pacific, Australia Protiea
e
5
1) Engler, 1892, 1897.
2) Wannan & Quinn, 1991.
3) Not placed in any family by Engler, 1883, 1897.
4) Does not include Solenocarpus with representatives in Tropical Asia.
5) Leenhouts, 1955; Forman et al., 1994.
Table 1. Genera included in analysis.
B. S. Wannan: Analysis of generic relationships in Anacardiaceae
169
Character polarities were determined by outgroup analysis (Maddison, Donoghue &
Maddison, 1984). Branch lengths were calculated using the ACCTRAN optimisation.
Only unambiguous character state changes were recorded on the branches in the final
figures.
Choice of taxa
Ideally terminal taxa should be species, so that both generic concepts and intergeneric
relationships could be tested in the cladistic analyses. Unfortunately, nonmolecular
data are not available for most of the species in the family. In fact, the full range of
characters has yet to be scored for a single species. The limited data that are available
have been assembled piecemeal by many workers as suitable material serendipitously
has come to hand. Hence, in order to obtain a preliminary estimate of the phylogenetic
signal in the available data, genera are used as the terminal taxa in the nonmolecular
analysis, with the data drawn from one or more species. Genera were chosen primarily
on availability of data, preferably from a number of authors. Thirty genera of Ana-
cardiaceae are included representing all five tribes (Engler, 1892) and both informal
subfamily groups (Wannan & Quinn, 1991). The outgroup for the analysis comprised
three genera from the Burseraceae (Bursera, Canarium and Garuga) representing the
three tribes (Leenhouts, 1955; Forman et al., 1994). The details of the genera used are
provided in Table 1. Sequence data were available for representative species of only
16 of the genera included in the nonmolecular analysis (Table 5). Exemplars of three
outgroups, Burseraceae, Rutaceae and Sapindaceae, were included, with trees being
rooted on the last two.
Additional information is provided below for some characters (Table 2)
(5) Leaves — The outgroup and most Anacardiaceae have imparipinnate leaves (b).
Fewer genera have simple leaves (a), though in some genera there are species with
both. Paripinnate leaves (c) are very uncommon, occurring in some species of genera
that possess mostly imparipinnate leaves. Bipinnate leaves occur only as polymorphic
character states in Spondias (S. bipinnata; Airy Shaw & Forman, 1967) and Bursera
(B. bipinnata; Porter, 1970) and have not been scored.
(9) Inflorescence structure — Few Anacardiaceae and Burseraceae have had their
inflorescence structure analysed (sensu Briggs & Johnson, 1979; Barfod, 1988). Most
descriptions do not accurately describe this character.
(10) Flower sex — Most genera of the Anacardiaceae, and probably Burseraceae, have
unisexual flowers (b), though frequently with the aborted remnants of the other sex
present. Fewer have bisexual (a) or polygamous (coded a & b) flowers. Botanists have
frequently confused the sex of flowers and it is likely that the flowers of some genera
which have been recorded as polygamous, and which have not been closely studied,
will be found to be unisexual. In many cases the male flowers are clearly unisexual
(with an aborted smaller ovary) while the female flowers appear to be bisexual but
the stamens have aborted anthers which are apparent only after sectioning (Wannan
& Quinn, 1992).
