The Evolution of Toxic Phenolic Compounds in a Group of Anacardiaceae Genera Author(s): Carlos J.

Aguilar-Ortigoza and Victoria Sosa Source: Taxon, Vol. 53, No. 2 (May, 2004), pp. 357-364 Published by: International Association for Plant Taxonomy (IAPT) Stable URL: http://www.jstor.org/stable/4135614 . Accessed: 20/02/2014 09:39
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TAXON 53 (2) * May 2004: 357-364

Aguilar-Ortigoza& Sosa * Compounds in Anacardiaceae

The evolution of toxic phenolic compounds in a group of Anacardiaceae genera

Carlos J. Aguilar-Ortigozal,2 & Victoria Sosal
SInstituto de Ecologia, A.C., Apartado Postal 63, 91000 Xalapa, Veracruz, MWxico.victoria@ecologia.edu.mx (author for correspondence) 2Facultad de Ciencias, Universidad Autdnoma del Estado de MWxico, Toluca, Mixico. aguilarc@ ecologia.edu.mx Anacardiaceae are largely tropical trees, shrubs and lianas of the order Sapindales, characterized by production of three types of toxic phenols: biflavonoids, alkylcatechols and alkylresorcinols. Anatomical, morphological and rbcL sequence data were used to reconstruct the phylogeny of a group of Anacardiaceae and address questions about the origin and evolution of these toxic phenolic compounds. Their evolutionary patterns are discussed in relation to the group of Hemipteran insects that feed on Anacardiaceae. Our study included 22 taxa

of Anacardiaceaeand the results supportpreviousphylogenetic studies in thattwo clades are detected:a basal
clade, with Spondias and related genera that do not produce toxic phenolic compounds, and a second clade with the remaining genera, i.e., those that produce biflavonoids, as do species of Burseraceae. The evolutionary patterns of alkylcatechols and alkylresorcinols are not straightforward; these substances are produced in

unrelatedgroupsof genera.We suggest, however,thatHemipteran insects do not feed on taxa of Anacardiaceae

that produce alkylcatechols. KEYWORDS: alkylcatechol, alkylresorcinol, Anacardiaceae, associated herbivores, biflavonoid, phylogenetics, evolution.

INTRODUCTION

Anacardiaceae are an angiosperm familyknownto in the resincanalsof prisubstances produce allergenic withtheveins of maryandsecondary phloemassociated leaves and other parenchymatous tissues (Metcalf & of threetypes: arephenols Chalk,1950).Toxicchemicals alkylcatechols, alkylresorcinols and biflavonoids. the mostallergenic andcommonof these,is a Urushiol, mixtureof saturated and unsaturated pentadecyl-and of taxa,suchas foundin a number heptadecylcatechols,
poison ivy (Toxicodendron radicans; Eggers, 1974;

In Anacardiaceae toxic phenolsare likely a defense the of restricting againstpests,becausetheyare capable (Cojocaru growthof pathogenic fungisuchasAlternaria & al., 1986;Harbome, 1999).It has alsobeensuggested thattoxic phenolsare a defenseagainstinsectsandvertebrates(Joel, 1980; Mitchell, 1990; Farrel& al., 1991).

of toxicphenolsin Anacardiaceae andrelatOccurrence interaced groupshave createdinteresting plant-insect tions. For example,Bursera,a groupclosely relatedto Anacardiaceae, producesterpenes against Coleoptera
such as Blepharida (Furth & Young, 1988; Becerra,

Gross & al., 1975; Baer & al., 1980; Adawadkar & & al., 1986; EISohly,1983;Du & al., 1984;Gambaro & al., 1997). Cardol,anotherallergenic Rivero-Cruz phenolic compound that is characteristicof some is a pentadecylresorcinol found in the Anacardiaceae,

thatBlepharida feed on 1997).It has also beenreported in which the severalspecies of Rhus (Anacardiaceae) toxic phenolsthat have been detectedwere flavonoids
(Furth & Young, 1988; Becerra, 1997). Calophya, a

feeds on speciesof monophagous genus of Hemiptera, Anacardiaceae and Rutaceae(Hodkinson, Burseraceae, fruit of the cashew nut (Anacardium occidentale; Tyman 1989). Coevolutionary hypothesesof the relationship & Morris,1967;Evans& Schmidt,1980).Heptadecyl- betweenCalophyaand some species of Anacardiaceae & Basset, resorcinol is foundin themangofruit(Mangifera indica) have recently been proposed(Burckhardt & al., 1986). Biflavonoidsare commonin 2000). (Cojocaru most groups of Anacardiaceae 80 genbut absent from the Fifty-two speciesof 27 of the approximately & al., era of Anacardiaceae containtoxic phenols (Mitchell, Spondias groupof genera(Young,1976;Wannan & al., 2003). The majorityof 1990; Aguilar-Ortigoza 1985; Young& Aist, 1987; Wannan& Quinn, 1988; Yuhthesetoxic speciesaremembers of tribeRhoeae. Meei & al., 1989). Biflavonoids are also common in the Engler (1883) divided Anacardiaceaeinto five gymnosperms (Smith, 1976) and in Burseraceae tribes: Anacardieae, Rhoeae,Semecarpeae (Wannan& al., 1985). Spondiadeae,
357

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Aguilar-Ortigoza& Sosa * Compounds in Anacardiaceae

TAXON 53 (2) * May 2004: 357-364

and Dobineae,basedon morphological characters such at anthesis andfruit,stylar as carpelandlocule number insertionof ovule, and leaf morphology. morphology, However,studiesbased on anatomical, morphological, thatthereareonly two andmolecular evidenceindicate lineageswithinthe family,one formed by the generaof witha few generaof Rhoeae,anda second Spondiadeae with the remaininggenera(Wannan & Quinn, 1991; Terrazas, 1994; Terrazas& Chase, 1996; Pell & Urbatsch, 2001). We used anatomical, morphological and rbcL of a groupof thephylogeny datato reconstruct sequence andotherspreviously generabelongingto Spondiadeae in Anacardieae and Rhoeae,and to address considered questionsabout the origin and evolutionof phenolic suchas alkylcatechols, toxiccompounds alkylresorcinols and biflavonoids. We discussthese compounds in relainsects that feed on tion to the group of Hemipteran Anacardiaceae.

and represent aspects of morphology and anatomy of

leaf, inflorescence, flower,fruit,seed and wood (Table datamatrix is proandanatomical 1;.the morphological
vided in Appendix 2 and the examinedherbariumspecimens in Appendix 3 (both available online). Chemical characters. - Occurrenceof alkylcatechols, alkylresorcinols and biflavonoids in different parts of the plants was taken for most species from the compilation of Aguilar-Ortigoza& al. (2003) (Fig. 1; Appendix 1). For some other species the same methods described in Aguilar-Ortigoza& al. (2003) were carried out to determine occurrence of these chemicals (Appendix 1). In cases where the informationwas taken from other sources, references are cited. Molecular methods. - DNA from fresh leaves

AND METHODS MATERIALS

and herbarium specimenswas extracted using the 2X of Doyle& Doyle(1987).TotalDNAand CTABmethod PCR products were cleaned with QIAquick silica to the manufacturer's columns(Qiagen,Inc) according in two overlapTherbcLexon was amplified protocols. to the PCRprotocolandtwo ping fragments according in Savolainen described & al. (2000a). pairsof primers
PCR products were sequenced in both directions with Mix Terminator these PCR primers,using the BigDyeTM and an ABI 377 automatedsequencer following manufacturer'sprotocols (Applied Biosystems, Inc.). Phylogenetic analyses and alignments. Three parsimonyanalyses were performed,morphology alone, rbcL alone, and a combined analysis. They were performedwith PAUP 2.0b2 (Swofford, 2000) and ana-

Plant material. - Our study includes only representatives of 22 out of the 80 genera of the family. However, our sampling strategy for the phylogenetic analysis was to include differentspecies of currentlyrecognized groups in Anacardiaceaeas well as species having any of the three toxic phenolic compounds consid-

molecular eviered in this study.Current phylogenetic dence indicates that Anacardiaceaeare sister to Burseraceae and that Sapindaceae, Rutaceae and & al., 2000a, Meliaceae are closely related(Savolainen as an outgroup, four b; Soltis & al., 2000). Therefore, species belonging to Burseraceae, Sapindaceae,
Rutaceaeand Meliaceae, were considered.Vouchersand DNA GenBank accession numbers are given in Appendix 1 (see online version of Taxon). Morphological characters. - The 88 morphological charactersused in the presentanalysis were compiled from our own observations of herbariummaterial and supplementedwith data in the literature. The characters are essentially those used by Aguilar & al. (2004)

(Fitch, 1971). The three lyzed using Fitch parsimony

analyses were heuristic searches performed with 1000 randomadditionsequence replicatesto look for multiple optimal-tree islands (Maddison, 1991). Analyses used TBR (tree bisection reconnection) branch swapping, MULTrees, steepest descent and ACCTRAN optimization. Internal support was evaluated with jackknife analysis (Farris& al., 1996) of 1000 replicates and 30% deletion of characters.In morphologicalanalysis characters were considered unordered. In molecular analysis contiguous sequenceswere assembledand checked using Sequencher 3.0 (Genecodes, Inc.); rbcL sequences are

andeasilyaligned by eye. lengthconserved

1o H

OH

OH

OH

OH
(CHz2)14CH3 (CH2)7CH=CH(CH2)7CH3

C15H31

(1) A 3-Pentadecylcatechol

(2) A 3-Heptadecylcatechol

(3) Pentadecyl resorcinolor Cardol

(4) Rhusflavanone,a biflavonoid

Fig. 1. Toxic chemicals in Anacardiaceae.

358

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TAXON 53 (2) * May 2004: 357-364

Aguilar-Ortigoza& Sosa * Compounds in Anacardiaceae

Table 1. Morphological, anatomical and phytochemical character and character-states used in the phylogenetic analyses of genera of Anacardiaceae.
48. Carpelnumber:0 = five, I = three, 2 = two, 3 = one. 1. Habit of plant: 0 = tree, 1 = shrub. 2 = simple. 49. Locules in ovary at anthesis: 0 = five, 1 = three, 2 = one. 2. Leaves: 0 = paripinnate,1 = imparipinnate, 50. Stylar insertion:0 = apical, 1 = ventral-lateral. 3. Leaf shape: 0 = oblong, 1 = elliptic, 2 = ovate, 3 = obovate. 51. Stigma morphology: 0 = capitate, 1 = spathulate. 4. Leaf texture:0 = chartaceous, 1 = coriaceous. 52. Ovule orientation:0 = epitropous, 1 = apotropous. 5. Leaf duration:0 = evergreen, 1 = deciduous. 6. Leaf grouping in branches:0 = sparsed, 1 = clustered at apex. 53. Ovules per locule: 0 = two, 1 = one. 54. Ovule integument:0 = two, 1 = one. 7. Leaf margindissection: 0 = serrate, 1 = entire. 55. Ovule insertion:0 = apical, 1 = apico-lateral,2 = latero-basal,3 = basal. 8. Rachis: 0 = not winged, 1 = winged. 56. Fruitform: 0 = ovoid, 1 = oblate, 2 = suborbicular. 9. Terminalleaflet shape: 0 = ovate, 1 = elliptic, 2 = obovate. 57. Winged fruit:0 = absent, 1 = present. 10. Apex of the leaf: 0 = acute, 1 = obtuse. 58. Peduncule of fruit: 0 = thin, 1 = thick. 11. Lamina type: 0 = dorsiventral,I = isobilateral. 59. Fruittrichomes:0 = absent, 1 = present. 12. Foliar epidermis:0 = single-layered, 1 = multi-layered. 60. Epidermisof exocarp: 0 = unlignified, 1 = lignified. 13. Foliar hypodermis:0 = absent, I = present. 61. Hypodermisof exocarp: 0 = absent, 1 = present. 14. Stellate trichomes:0 = present, 1 = absent. 62. Mesocarp sclereids with resin canals: 0 = absent, 1 = present. 15. Capitatetrichomes:0 = present, 1 = absent. 63. Mesocarpwith inner parts lignified: 0 = absent, I = present. 16. Cuticularstriae:0 =random, 1 = radial. 64. Endocarpnumberof layers: 0 = one, 1 = two, 2 = three, 3 = four. 17. Giant stomata:0 = absent, 1 = present. 18. Type of venation: 0 = camptodromous,1 = craspedodromous. 65. Endocarpdiscrete fourth layer: 0 = absent, 1 = with parenchyma, 2 = with sclereids. 19. Size of primaryvein: 0 = massive, 1 = stout. 66. Endocarpcrystals in the layer: 0 = absent, 1 = present. 20. Angle of secondaryvein: 0 = narrow,1 = moderate. 67. Endocarpdiscrete third layer: 0 = absent, 1 = with palisade-shaped 21. Tertiaryveins: 0 = percurrent,1 = reticulate,2 = ramified. 22. Marginalvenation: 0 = fimbriate, 1 = incomplete. sclereids, 2 = with sclereids. 68. Endocarpdiscrete second layer: 0 = absent, I = with palisade-shaped 23. Veinlets: 0 = simple, 1 = branched. 24. Inflorescence position: 0 = terminal, 1 = axilar. sclereids, 2 = with osteosclereids, 3 = with brachysclereids. 69. Endocarpdiscrete first layer: 0 = with sclereids, 25. Inflorescence type: 0 = panicle, 1 = thyrsoid. I = with palisade-shapedsclereids. 26. Cupularinvolucre:0 = absent, 1 = present. 70. Endocarpfirst layer size: 0 =less the twice of rest of layer, 27. Flower sex: 0 = unisexual, 1 = bisexual. 28. Sepal number:0 = three, 1 = four, 2 = five, 3 = six. 1 = more than twice thickness. 71. Number of seeds: 0 = five, 1 = three, 2 = two, 3 = one. 29. Calix aestivation:0 = valvate, 1 = imbricate. 72. Embryo:0 = straigth, 1 = curved. 30. Sepal indument:0 = glabrous, 1 = pubescent. 73. Testa:0 = membranous, 1 = crustaceous. 31. Margin sepal indument:0 = glabrous, 1 = pubescent. 74. Endosperm:0 = present, 1 = absent. 32. Sepal shape: 0 = oblong, 1 = ovate. 75. Cotyledon margin:0 = lobed, 1 = entire. 33. Petal number:0 = five, 1 = four, 2 = zero. 76. Wood parenchymaapotracheal:0 = absent, 1 = present. 34. Corolla aestivation:0 = imbricate, 1 = valvate. 0 = alliform, 1 = banded, 2 = vasicentric. 77. Wood parenchymaparatracheal: 35. Petal shape: 0 = oblong, I = elliptic, 2 = ovate. 78. Wood ray width: 0 = 1-5 cells, 1 = 6-10 cells. 36. Stamen number:0 = ten, 1 = five, 2 = eigth. 79. Wood ray type: 0 = heterogeneous IIB, 1 = heterogeneous IIA, 37. Filament form: 0 = filiform, 1 = subulate. 2 = heterogeneousIII. 38. Filament indument:0 =glabrous, 1 = pubescent. 80. Septate wood fibers: 0 = present, 1 = absent. 39. Anther form: 0 = pyriform, 1 = rotund,2 = botuliform. 81. Resin canals in wood rays: 0 = present, 1 = absent. 40. Anther:0 = basifixed, I = dorsifixed. 82. Resin canals in ploem: 0 = absent, I = present. 42. Pollen shape: 0 = prolate, 1 = spheroidal. 83. Vessel clusters: 0 = absent, 1 = present. 42. Pollination:0 = by insects, 1 = by wind. 84. Starchin vessels: 0 = absent, 1 = present. 43. Nectariferousdisk: 0 = intrastaminal,1 = extrastaminal. 85. Growthring: 0 = absent, 1 = present. 44. Disk form: 0 = patelliform, 1 = cotyliform, 2 = columnar. 86. Alkylcatechols: 0 = absent, I = present. 45. Disk margin:0 = crenate, 1 = lobate. 87. Alkylresorcinols:0 = absent, 1 = present. 46. Number of disk lobes: 0 = ten, 1 = five. 88. Biflavonoid: 0 = absent, 1 = present. 47. Carpellodenumber:0 = five, 1 = three, 2 = two, 3 = one.

Reconstructing the history of chemical characters. - To investigate the evolutionary history of chemical characterswe mappedthe presence of each of the three phenolic compounds (alkylcatechols, alkylresorcinols and biflavonoids) on the strict consensus tree using parsimonyoptimizationand the TRACE option of MacCladeversion 3.04 (Maddison& Maddison, 1992).

RESULTS
Phylogenetic relationships. Morphological

analysis recovered a single equally most-parsimonious tree (MPT) of 453 steps, with a consistency index (CI) of 0.38 and a retentionindex (RI) of 0.52, including a total of 88 characters,with 86 parsimonyinformativecharac359

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& Sosa* Compounds in Anacardiaceae Aguilar-Ortigoza

TAXON 53 (2) e May2004:357-364

ters. Fig. 2 represents one of the MPT selected at random. rbcL analysis recovered21 MPT of 481 steps, with a CI of 0.73 and a RI of 0.61, including 1414 characters, with 127 parsimonyinformativecharacters.Fig. 3 represents one of the MPT selected at random.Matrixof combined analysis included 1502 characterswith 213 parsimony informative characters.Eight MPT of 1002 steps were obtainedwith a CI of 0.57 and a RI of 0.53. Fig. 4 representsone of the MPT,selected at random.Topology of MPT is very similar in the three analyses. The morphological tree is the least supported,with only a few clades receivingjackknife supportabove 50%. In the tree analyses the Anacardiaceae clade is always recovered with good jackknife support.In the three analyses, Clade I and Clade II are recovered.Buchanania is always basal in Clade II and Anacardiumand Mangifera form a subclade. Position of some of the membersof Clade II varies (Figs. 2-4). For example, Blepharocaryais in a subclade with Anacardium and Mangifera in the rbcL analysis while in the combined analysis it is in a subcladewith the rest of the taxa of Clade II. The best supportedtopology is from combined analysis in which the Anacardiaceae clade is well supported (100% jackknife value). Two clades are found within the family: a well supported basal clade formed by Cyrtocarpa, Spondias and Tapirira,and a second clade with the rest of the genera
Bursera aRuta Dodonaea Svetenia 62 57 Tapirira Cyrtocarpa Spondias Buchanania Blepharocarya Anacardium Mangifera Bonetiella Cotinus Actinocheita Comocladia Metopiumr Amphipterygium Pistacia Pseudosmodingium Mosquitoxylum Schinopsis Astronium Schinus Rhus Smodingium Toxicodendron M c < u 0

Bursera Ruta Dodonaea Swietenia 62 Tapirira

-E

Cyrtocarpa Spondias Buchanania Blepharocarya Anacardium

83

Mangifera Bonetiella Cotinus Actinocheita Comocladia Metopium Amphipterygium Pistacia Pseudosmodingium Mosquitoxylum Schinopsis Astronium Schinus Rhus Smodingium Toxicodendron

Fig. 3. One of the 21 MPTtrees of the rbcL analysis of 481 steps, with a Cl of 0.73 and a RI of 0.61. Jackknife percentages (>50%) are indicated above the branches.

(strongly supported90% jackknife value). Buchanania appears basal in this clade. Well supported groups in these clade are formed by Actinocheita, Bonetiella and Comocladia (jackknife value of 94%), Metopium and Mosquitoxylum (97%) and Astronium and Schinopsis Character evolution. - Evolution of the chemical charactersshow different patternsdepending on the type of toxic phenolic compound. Alkylcatechols evolved in two groups in Anacardiaceae,in a clade (not supported) formed by Actinocheita, Astronium, Bonetiella, Comocladia, Metopium, Mosquitoxylum, Pseudosmodingiumand Schinopsis, and in a subclade (well supported) formed by Smodingium and Toxicodendron.The ancestral condition is the lack of alkylcatechols (Fig. 4). The presence of alkylresorcinols is restrictedto the clade of Anacardiumand Mangifera and in Schinus (Fig. 4). Biflavonoids arose independently in Burseraceaeand in Clade II of Anacardiaceaewith the exception of Buchanania (Fig. 4).

(100%).

Fig. 2. MPT tree of the morphological analysis of 453 steps, with CI of 0.38 and a RI of 0.52. Jackknife percentages (>50%) are indicated above the branches. 360

DISCUSSION
Phylogenetic analysis. Our results agree with

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TAXON 53 (2) e May 2004: 357-364

Aguilar-Ortigoza& Sosa * Compounds in Anacardiaceae

Ej 0 Dodonaea 80

130 Ruta
O0 Swietenia M0 Bursera
90

Outgroup

Tapirira

S65 E0loo
90 97

0 Cyrtocarpa
0O Spondias =0 Buchanania

Clade I

me Anacardium
WM Mangifera

0M

0 Blepharocarya 72

M 0 Cotinus
M10 Amphipterygium Pistacia 6me
8Q O0 M80

Schinus
Rhus

Clade II

91

M 0 Smodingium
M0 94 Toxicodendron Actinocheita 0Bonetiella M( Comocladia

84

97

0 Metopium
0 Mosquitoxylum 6

O Absenceof biflavonoids M1 m Presenceof biflavonoids 100 andalkylresorcinols O Absenceof alkylcatechols O Presenceof alkylcatechols * Presenceof alkylresorcinols

Pseudosmodingium

M 0 Astronium M @ Schinopsis

Fig. 4. One of the eight MPTof the combined analysis of 1002 steps with CI = 0.57 and RI = 0.53. Jackknife percentages (>50%) are indicated above the branches. Evolution of alkylcatechols, alkylresorcinols and biflavonoids are mapped onto the tree.

previous phylogenetic studies (e.g., Gadek & al., 1996), in thatAnacardiaceaeare a monophyleticgroup.The two lineages in Anacardiaceaementioned in our results are also detected in molecular phylogenetic studies (Miller & al., 2001; Pell & Urbatsch, 2001) and in studies that combined charactersets (DNA sequences and morphology, Terrazas& Chase, 1996). Furthermore, endocarpand wood charactersalso indicate two groups in the family, comprised of the same genera (Wannan& Quinn, 1990, 1991). Two types of endocarp are found in Anacardiaceae, the Anacardium-type(with discrete and regularly arrangedlayers), three or fewer carpels and a unilocular ovary, and group B with the Spondias-type of endocarp (a thick mass of usually lignified and irregularlyoriented sclerenchyma),more than three carpels and a multilocular ovary. Group B corresponds to tribe Spondiadeae from Engler's (1883) classification or to Clade I, including Antrocaryon, Cyrtocarpa,Dracontomelon, HaemaLannea, Sclerocarya,Spondias tostaphis,Harpephyllum, and Tapirira,among others. The Spondias clade retained plesiomorphiccharacterssuch as a gynoecium with five carpels, fruit often multilocular with a thick endocarp, lignified, andwith irregularlyorientedsclereids (Wannan & Quinn, 1990). The Spondias-type of endocarpis also present in some Burseraceae(Wannan& Quinn, 1990). The genera of Clade II share morphologicalcharacters such as a tricarpelar gynoecium, unilocularfruitwith
C. nigridorsalis C. C. rhois duvauae

Burseraceae .--Sapindaceae
Meliaceae

Rutaceae Tapirira Cyrtocarpa Spondias Buchanania Anacardium Mangifera Blepharocarya Cotinus Amphipterygium Pistacia Schinus Rhus Smodingium Toxicodendron Actinocheitaorbicola Bonetiella Comocladia Metopium Mosquitoxylum Pseudosmodingium Astronium Schinopsis L

C. evodiae C. nigrilineata C. monticola -C. longispiculafa

C. spondiasiae C. verrucosa C andina C. clausa C. mammifex C. patagonica C rubra C. orbicola C. gallifex C. schini C. scrobiocola C. catillicola C. hermicitae C. terebinthifolii

Fig. 5. Feeding preferences of Calophya species (right) on Anacardiaceae, Burseraceae and Rutaceae hosts (left). Calophya phylogeny based on Burckhardt & Basset (2000). 361

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Aguilar-Ortigoza& Sosa * Compounds in Anacardiaceae

TAXON 53 (2) e May 2004: 357-364

an endocarpcomposed of discreteandregularlyarranged layers of cells (Wannan& Quinn, 1990). One of the well supported subclades in Clade II is formed by Schinus, Rhus, Smodingium and Toxicodendron.They all share characterssuch as imparipinnate leaves sparsely distributed along branches, ovate and chartaceous leaflets; moreover, they have the same calyx indument,thyrsoid inflorescence and wood having the heterogeneous IIB are cosmopolitan, type of ray. Rhus and Toxicodendron while Schinus is from SouthAmerica and Smodingiumis endemic to South Africa. The other subclade, also well supported, is formed by Actinocheita, Bonetiella and Comocladia. These three neotropicalgenera share characters such as coriaceous leaves, panicle type of inflorescence with axillar insertion and imbricatecalyx aestivation. Actinocheitaand Bonetiella are endemic to Mexico, and Comocladia to Mexico and the West Indies. Metopiumand Mosquitoxylumare a sister group distributed in Mexico and the West Indies. The closely related group formed by Pseudosmodingium, Astronium and Schinopsis is also neotropical. Character evolution. - One of the most inter-

independentlyat least twice, in the clade of Anacardium + Mangiferaand in Schinus. These phenolic compounds are synthesized in the pericarps of three economically occidenimportantspecies: the cashew nut (Anacardium tale), the mango (Mangifera indica) and the less widely Their known Brazilianpepper (Schinus terebinthifolius).

in certain fruitshave been reported to cause dermatitis individuals 1978, 1981). (Morton, Spondiaswhich does not producealkylcatechols,
alkylresorcinolsor biflavonoids has the capacity to synthesize phenolic compounds (Corthout & al., 1989). Spondias mombin L. has been reported to possess the

sincethe thesesubstances, metabolic routeto synthesize

precursors of the formation of a related phenol, hephave been detected (Corthout& al., tadecadienyl-phenol, 1989). Biosynthetic routes of alkylcatechols and biflavonoids are involved in the shikimatepathway(VanSumere, 1989). Accumulation of alkylcatechols, alkylresorcinols and biflavonoids is in some cases restricted to certain organs of the plant. Alkylcatechols and biflavonoids are usually present in leaves and bark. But in some species of evolutionof the toxic phenoliccom- such as Metopiumbrownei alkylcatechols also found in estingpatterns pounds in Anacardiaceae is that shown by the wood (Young, 1976). A few Semecarpus species (not in included in our analysis) also produce alkylcatecholsin includedas an outgroup biflavonoids.Burseraceae, & al., 1980). Occurrenceof these chemas sisterto Anacardiaceae fruits(Carpenter our analysesand recognized & Chase, 1996; Pell & icals in only certainorgansof the plant can be explained (Gadek& al., 1996; Terrazas in terms of enzyme specificity and substrates. Schwab Urbatsch, 2001), synthesizes biflavonoids. These biflavonoids are not producedby the generaof Clade I of (2003), in a review of metabolome diversity, concluded is causedby low enzyme that diversityof metabolites Anacardiaceae, the Spondiadeae of Engler (1883), but specificity but availability of suitable substratesdue to they are produced in the taxa of Clade II, arising only has also been taken into account. once in the historyof the group.Wannan& al. (1985) and compartmentation It has been documentedthat in Anacardiaceae,alkylYoung & Aist (1987) previously pointed out this pattern. catechols are toxic and repellent,and hence an effective the genera of Clade I did not produce the Furthermore, defense system against herbivory by insects (Farrell& phenolic compounds we considered. The members of Clade II, with the exception of Buchanania, synthesize al., 1991). The diversificationof certaingroupsof insects biflavonoids. The presence of this compound strongly as a resultof a feeding relationshipwith certaingroupsof plants has been reported for a number of groups, e.g., supports the inclusion of Amphipterygium and Blepharocarya in Anacardiaceae,although these genera Phyllobrotica (Chrysomelidae)and Lamiales (Farrel& have been considered in Julianiaceaeand Blepharocary- Mitter, 1990; Mitter & al., 1991); Blepharida aceae, respectively (Airy Shaw, 1965; Hemsley, 1908). (Chrysomelidae) and Bursera (Becerra, 1997). Among Lamiaceae, species of genera such as Stachys, Amphipterygium's flowers lack a corolla and Blepharocarya possesses small globose inflorescences Physostegia and Scutellaria produce toxic iridoid (terand their leaves are opposite and pinnate, charactersnot penoids) compounds that restrain several herbivores common among Anacardiaceae. (Farrel & Mitter, 1990). However, species of The evolutionary patterns of alkylcatechols and Phyllobroticafeed on species of these Lamiaceae(Mitter & al., 1991). Phyllobrotica is a genus strictly monoalkylresorcinols in the members of Clade II are not Alkylcatechols evolved in two groups: phagous (Farrel & Mitter, 1990; Mitter & al., 1991). straightforward. in a clade formed by Actinocheita, Astronium, Bursera species producepinene, camphene,phelandrene Bonetiella, Comocladia, Metopium, Mosquitoxylum, and limonene (terpenes) in resin canals. These terpenes Pseudosmodingium and Schinopsis, and in a subclade are toxic to most herbivores. However, species of the formed by Smodingiumand Toxicodendron. monophagousgenus Blepharida feed on certainBursera Alkylresorcinols are less common than alkylcatespecies dependingon a specific terpene (Becerra, 1997). Burckhardt & Basset (2000) indicatedthatthe diverchols or biflavonoids among Anacardiaceae.They arose
362

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TAXON 53 (2) e May 2004: 357-364

Aguilar-Ortigoza& Sosa * Compounds in Anacardiaceae

sification of the hemipterangenus of insects, Calophya, is closely relatedto the plants they feed on. Theirphylogenetic study of Calophya corroboratessuch relationships, suggesting that these hemipteran insects are monophagous and only feed on species of the related groups of plants such as Anacardiaceae, Rutaceae and Burseraceae(Burckhardt & Basset, 2000). According to their results, Calophya evodiae feeds on Rutaceae, C. nigrilineata feeds on Burseraceae, C. spondiasiae on Spondiaspinnata, C. longispiculata on Buchanania lanzan, C. rhois on Cotinus coggygria, C. nigridorsalis on Rhus trichocarpa; and more than ten species of Calophyafeed on species of Schinus.When the two phylogenies of Calophya and Anacardiaceae with their closely related groups are compared (Fig. 5), it can be shown that species of Calophya feed mainly on taxa of Rutaceae and Anacardiaceaethat are not capable of producing toxic phenolic compoundssuch as alkylcatechols. However, Calophya species are capable of feeding on taxa of Burseraceae, Rutaceae and Anacardiaceae that producebiflavonoid andresorcinolphenolic compounds. Most species of Calophyaare found to feed on species of Schinus that do not produce alkylcatechols but can synthesize alkylresorcinols and biflavonoids (Fig. 5). Further information is needed to test whether other groups of insects are capable of feeding on Anacardiaceae that produce alkylcatechols. Bioessays are also needed to confirm feeding preferences of Calophya species.

ACKNOWLEDGEMENTS
The projectwas madepossible by a grantfrom CONACYT Mexico (225260-5-29378Nto VS) and from PROMEP(to CJAO). We thankFranciscoLoreafor his help in obtainingherbarium specimens, and RauilAcevedo, Sergio Avendailo and Santiago Barriosfor their help with field work. We are gratefulto Bianca Delfosse for editingthe Englishversionof this manuscript.

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