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PHYLOGENETIC ANALYSIS OF HUMIRIACEAE WITH NOTES ON THE MONOPHYLY OF

Claudia Petean Bove

Depto. de Ciências Naturais, UNI-RIO, Rua Frei Caneca 94,5° andar, 20211-040 Rio de Janeiro RI, Brazil.

Abstract. Bove, C.1~ Phylogenetic analysis o[ Humiriaceae with notes on the monophyly o[ Ixonanthaceae. ].Comp.Biol. 2(1):19-24. A cIadistic analysis was applied to determine phylogenetic relationships of genera in the Neotropica! tàmily HlImiriaceae. Twenty-four om of fifty-tWo characters on morphology, anatomy, palynology, ontogeny and chemotaxonomy cOllld be polarized by the mllltiple omgrollp comparison method. Monophyly of the family is confirmed by three synapomorphies involving morphology of androecillm and fruit, and wood anatomy. Monophyly and relationships of the eight HlImiriaceae genera are sllpported by several synapomorphies. The present phylogenetic hypothesis is in accordance with the following parenthetical notation tree: (Tímtanea ( (( ( + » + (Hylocarpa (Duckesia + Endopleura»»). The monophyly of the proposed sister grollp Ixonanthaceae is supported by the apomorphic condition of free stall1ens and sell1i-inferolls ovary.

Key Words. HlIll1iriaceae; Ixonanthaceae; Phylogenetic Systematics. Introduction paid more attention to the structure of the fruit, whereas this kind of information was lacking in The Humiriaceae are a relativelysmall family previous papers. He described two tribes of flowering in the order Linales (Vántaneoideae and Humirioideae) which are (Cronquist, 1981) comprising 61 species (many coincident with the basic groups mentioned by subspecies, varieties and forms) in eight genera. Urban, 1877), elevatedthe subgenera cited above Ir has a Neotropical distribution, ranging from to the genera rank, and described three otl1er Nicaragua to Southern Brazil (Burger & . genera (Duckesia) Endopleura and Hylocarpa), Zamora, 1991). One species, Sacoglottis many species and intraspecific taxa. gabonensis (Baill.) Urb., however, is found in The earliest fossil records of the Humiriaceae Western Africa. The family has a marked were found in late Eocene (36,5 - 53 M.y.) in concentration in the Amazon forest, but also several countries of tropical South America occurs in the Atlantic forest, restingas,cerrados, (Cuatrecasas, 1961). The first fossil record found and campinaranas; it is rarely found in the in Brazil is from the Miocene (5,3 - 23,5 M.y.) semideciduous forest and on the rupestrefields. ofBahia State (Selling, 1945). It is a tàmily of woody, evergreen species,varying Planchon (1848), who considered closer from small shrubs to large trees. affinities between woody members of the Aublet (1775), Lamarck (1792), andMartius Linaceae ( Planch.) and (1827) described the earliest species of Erythroxylaceae, was the first to propose Humiriaceae, but Jussieu (1829) was the first phylogenetic relationships among the to consider this group as a family rank taxon. Humiriaceae. Bentham & Hooker (1862) Bentham (1853), recognizing three genera proposed the Linaceae series Planch. ( Aubl., Humiria St. Hil. and (Ixonanthaceae according to Cronquist, 1981) to Sacoglottis Mart.), published a precise and be closely related to the Humiriaceae. Baillon synthetic account ofthis family. Urban (1877) (1874) included this familyin the Linaceae (series provided a great contribution to the systematics Houmiriae Baill.) and related it to Ixonanthes Jack. of the family, creating a new concept of and Benth. (Erythroxylaceae). classitication based on the number and structure Hallier (1923) and Wrinkler (1931) followed of tl1e stamens, number of ovules in the ovary Baillon (1874) on the inclusion of the and position of carpels. He divided the family humiriaceous taxa in the Linaceae. Cuatrecasas into two basic groups (Vántanea and Humiria (1961) concluded that the Humiriaceae form a + Sacoglottis),and described three subgenera of natural and well-defmed group, perfectly separate Sacoglottis (Humiriastrum) Schistostemon and from the Linaceae, and closely related to Eusacoglottis). A taxonomic revision by Ixonanthes)OchthocosmusBenth. and Ctenolophon Cuatrecasas (1961), with a detailed Oliv. morphological investigation on various aspects, A phylogenetic analysis among the

,. Bove

Table 1. Characters and characters states used for cladistic analysis of Humiriaceae. 0= plesiomorphic state; 1,2= apomorphic states. CHARACTER CHARACTER STATE

1. Ellagic acid 0= absent 1 = present 2. Corolla aestivation 0= imbricated or contorred 1 = quincuncial or cochlear 3. NUll1ber of stall1en circles O = one 1 = two 2 = three or four 4. Stamen concrescense O = united 1 = free 5. Sterile stamens 0= absent 1 = present 6. Trifurcate stall1ens 0= absent 1 = present 7. Anthers thecae number O = two 1 = four 8. Connective shape O = with appendix 1 = withour appendix 9. Anther surtàce O = glabrous 1 = pilose 10. Locus nUll1ber per anther 0= bilocular 1 = unilocular 11. Dicolporate pollen grains O = absent 1 = present 12. Aperrure size on pollen O = longicolpate 1 = brevicolpate 13. Pollen grains sçulprure 0= LO partem 1 = OL partem 14. Size of colull1ella 0= consplCuous 1 = 1I1COnSplcuoUS 15. Nectariferous disc 0= extrastaminal 1 = intrastaminal 16. NUll1ber of stigmas O = two or more 1 = one 17. Ovary position O = superous 1 = semi-inferous 18. Number of traces in carpels 0= three 1 = tive 19. Number of ovules per loculus O = two 1 = one 20. Endocarp rype O = not woody 1 = woody 21. Foramen in the endocarp 0= absent 1 = present 22. Resiniferous cavities in the endocarp 0= absent 1 = present 23. Valve size of the fruit 1 = long 2 = short 24. Wood vesscl clell1ents O = sill1ple 1 = scalariform

Humiriaceae genera was undertaken by of Humiriaceae, determined by the sharing of Cuatrecasas (1961) but concentrated on 'grades' derived characters. rather than 'clades'. He identified various trends of character evolution, considering each Materiais and methods primitive or derived, according to the characters analyzed. This paper presents a cladistic anaIysis of The purpose of the present paper is to present Humiriaceae using principIes of phyIogenetic a hypothesis of relationships between the genera systematics (Hennig, 1966) based on data fram

20 ]. Comp. Biol. 2(1) 1997 Phylogcnctic Analysis of thc Humiriaccac

Table 11. Character states for Humiriaceae and the outgroups. Order to /ist the outgroups taxa is the least to the c/osest related and the Humiriaeeae taxa is alphabetieal. Missing data are indicated by question marks.

1 6 11 16 21 Erythroxylaccac 00000 00000 OOOO? OO?PO OO?O Linaccac+ Hugoniaccac OOPOO 00000 OOPOO 00000 OO?P Ixonanthaccac 10010 00000 00101 11?OO OO?O Duckesia 1?110 10110 10000 11071 1111 Endopleura 10100 01101 00001 10111 1021 Humiria 11000 00111 11011 10001 1011 Humiriastrum 10000 00101 10001 10111 1121 Hylocarpa 10101 00101 ?0001 10?11 0011 Sacoglottis 11000 00101 10001 10111 0111 Schistostemon 10000 10101 00001 10111 0111 Utntanea 10200 00100 00001 10001 0011

the morphology, anatomy, palynology, ontogeny applying the implicit enumeration option for and chemotaxonomy. The cytological and calculatingallpossible shortest trees. Allmultistate ecological data were not polarized. These characters were treated as unordered, or characters were derived fram material used as maximally connected (Slowinski, 1993). the basis for a palynological treatment of the family (Bove, 1996) and fram the following Results and discussion publications: Erdtman (1952), Cuatrecasas (1961), Saad (1962), Sharma (1962), Metcalfe The monophyly ofHumiriaceae is supported etal. (1968), Raj &Suryakanta (1968),Narayana in this study by at least three synapomorphies: & Rao (1969, 1973a, 1973b, 1976, 1977), stamens with thick connectives, fleshy,apiculum Oltmann (1971, 1975a, 1975b), Salgado- or linguiform appendix, fruits with a woody Labouriau (1973), Satabié (1974), Barth & endocarp and wood vessel elements with Barbosa (1976), Markgraf & d'Antoni (1978), scalariform perforation plates. Ixonanthaceae is Ybert (1979), Cronquist (1981), Pum & Den hypothesized to be the sister group of Breejen (1981), Lobreau-Callen et alo (1984), Humiriaceae, and both families share the Kool (1988), Van der Ham (1988), VanHooren following synapomorphies: intrastaminal freedisc & Nooteboom (1988), Yunus & Nair (1989). girding ovary, entire stigma, and presence of Palynological preparations were made following ellagic acid. Among the Linales, only the the methods ofErdtman (1952), and terminology Ixonanthaceae present freestamens, semi-inferior follows Punt et alo(1994). ovaries and pollen grains with supratectal spines, Character polarities for 24 characters selected thus herein interpreted as an apomorphic as informative, fram over 50 investigated, were diagnostic feature for this family, supporting its determined by the multiple outgroup comparison monophyly. method (Maddison et al., 1984) so as to detect The characters selected as informative are autapomorphies of sister graups and minimize presemed ascoded plesiomorphic or apomorphic misimerpretation ofcharacter states. This study states (TableI). TableII comains the data matrix comprises two levelsof outgroup: the sistergroup used in this analysis. There is only one most (Ixonamhaceae), and the closest outgraup of the parsimonious cladogram (Fig. 1) supported by clade Ixonanthaceae+ Humiriaceae (Hugoni- the data matrix presented in Table lI. The aceae and Linaceae); in cases of polymorphic cladogram is 32 steps long, with a consistency characters within these taxa, plesiomorphic states index of 78 and a retention index of 75. were inferred as those occurring in a third, more The division of Humiriaceae (clade A) imo remote, outgraup (Erythraxylaceae). two tribes, asoriginally praposed by Cuatrecasas The numerical cladistic analyses were (1961), is supported in the present study. performed with the phylogenetic inference Vantaneoideae, induding only Vimtanea, is software, Hennig86 version 1.5 (Farris, 1988) characterized by the stamens arranged in three

J. Comp. Bio/. 2(1) 1997 21 Bove

Table 111. Distribution of apomorphic character states of Humiriaceae based on the phylogenetic hypothesis in Figure 1. The number of characters follows thosepresented in the texto Clades follow figure 1. C<*"indicates character with homoplastic appearance in the cladogram. Synapomorphies Autapomorphies Clades Characters Genera Characters

A 8,20,24 Duckesia 5*,22 B 9 Endopleura 23* C 18,19 Humiria 2*,9,11*,12,14,21* D 22* Humiriastrum 21*,23*,25 E 3.2 Hylocarpa 5* F 11* Sacoglottis 2* G 7,21* Schistostemon 6 Vántanea 3.1

or four circles (character # 3). It is interesting (fruits with long valves-7fruits with short to note that Oltmann (1971) disagreed with the valves). The absence of resin in resiniferous placement of Thntanea in a monotypic tribe, at cavities of the fruits is observed only in that time based solely on palynological evidence. Humiriastrum) and corresponds to the unique The Humirioideae (clade B), comprising all non-homoplastic autapomorphy of this genus remaining genera of the family, are defined by (character # 25). unilocular anthers (character # 10). The presence of sterile stamens in Duckesia The tribe Humirioideae includes six clades. and Hylocarpa is supported by two equally The first clade, comprising only Humiria, is parsimonious hypotheses: this character state supported by three synapomorphies (hairy thecae, could either be a parallelism or a synapomorphy pollen grains with a short colpus, inconspicuously of clade E (Duckesia+ Endopleura + Hylocarpa), columellate exine) and three homoplastic with reversion in Endopleura. This latest characters (quincuncial or cochlear corolla explanation for the sterile stamens would be the aestivation, dicolporate pollen grains, and only reversal observed in the phylogeny of the foraminate endocarp). Clade C (Duckesia + Humiriaceae. Endopleura + Humiriastrum + Hylocarpa + The present phylogenetic analysis indicates Sacoglottis+ Schistostemon)is supported by five genera defined by unique apomorphic states trace carpels, and ovary with uniovulate cells. A (synapomorphies cited above for Humiria, basal division in clade C includes a pair of sister Humiriastrum) Thntanea)and Schistostemon,this groups. Duckesia) Endopleura and Hylocarpa latter genus diagnosed by the presence of (clade E) are hypothesized to be more closely trifurcate stamens). The remaining genera have related among themselves by sharing the monophyly weakly corroborated by homoplastic apomorphic state of stamens arranged in two character states. There are well-defined clades whorls. Duckesia and Endopleura (clade G) are (A, B, C, E, G) as well as weakly defined clades sister taxa based on the presence of anthers with (D, F) (Table III). four thecae and a foraminate endocarp. The The Humiriaceae were formerly treated either remaining clade D (Humiriastrum, Sacoglottisand as partofLinaceae (Baillon, 1874; Hallier, 1921; Schistostemon)ishypothesized to be monophyletic Wrinkler, 1923) or as an independent family by the synapomorphic resiniferous cavitiesin the (Jussieu, 1829; Bentham, 1853; Cuatrecasas, endocarp. A sister group relationship between 1961, Cronquist, 1981). Three synapomorphies Humiriastrum and Sacoglottis (clade F) is showed herein support the second hypothesis. supported by the presence of dicolporate pollen The earliest hypotheses of"relationships" among grams. the Humiriaceae, proposed by Planchon (1848), The valve size of the fruit was included in the Bentham & Hooker (1862) and Baillon (1874), character analysis, although it could not be are conceptually incongruent with the cladistic polarized (outgroups not presenting valveson the principles of monophyly. The authors mentioned fruit~). The direction of the transformation series above relate the family Humiriaceae with only a is indicated by the final cladogram topology part (one genus) of other families (Linaceae and

22 J. Comp.Biol.2(1) 1997 PhylageneticAnalysisaf the Humiriaceae

CJ.) (ti CJ.) U (ti c: o CJ.) C) (ti ::::J CJ.) CJ.) (ti 5 u I Q) E (ti + u 2 . E >. (ti (U (U :::se CJ.) 1i5 . x (ti ... (1) e- CI) Q) c: t:: .(U .(U o (U e u as .S;; .S;; - (.) (1) ~ (ti c: .!!2 o g. ~ c: § § (.) .t: :::s "O w :::i :x: :x: :x: c Li)

F G

o E

C

B

A

Figure 1. Cladogram depicting the phylogenetic relationships among Humiriaceae genera and outgroups, result- ing fr01n the parsimony analysis of the data matrix of Table 11. Synapmnorphies are listed in the text and Table I.

Erythroxylaceae). Thus the Humiriaceae became group of all remaining genera of the family. a paraphyletic group. This hypothesis is refuted Cuatrecasas (1961) established several different in the present paper. relationships among genera, based on individual The phylogenetic relationships within the series of character transformations, usually family have been poorly understood along this comparing two genera at a time. He considered century, usually considering degrees of overall Sacoglottis as the most derived genus, based similarity, producing phenetic rather than entirely on the reduction in the number of phylogenetic classifications. Cuatrecasas (1961) stamens. discussed possible lines of evolution of each of his characters based only on morphological data. Acknowledgments. I am deeply grateful to Dr. He pointed out that Vántaneawould be the most Wilson Costa for his teaching ofthe fundamental~ ancient of the family, a hypothesis herein of phylogenetic systematics, providing valuable corroborated; Vántanea appears as the sister suggestions, and for bis constant encouragement.

J. Comp.Biol. 2(1) 1997 23 Bove

Special thanks are due to Dr. Therezinha d'allantospermun borneense forman et d'allantospermun Sant'Anna Melhem for her guidance in pollen Multicaule (Capuron) Nooteboom. Adansonia 8(3):337-351. analysis. I am indebted to Dr. Rubens Pirani for NARAYANA,L.L. & D. RAO. 1969. Conrributions to the his reading of a previous version of the floral anatomy ofHumiriaceae 1. J. Jap. Bot. 44:328- manuscript. This research was supported by 335. Coordenação de Aperfeiçoamento de Pessoaldo NARAYANA,L.L. & D. RAo. 1973a. Conrributions to the floral anatomy ofHumiriaceae 2. I. Jap. Bot. 48:143- Ensino Superior (CAPES) of the BrazilianFederal 146. Government. NARAYANA,L.L. & D. RAo. 1973b. ContribUtions to the floral anatomy ofHumiriaceae 3. I. Jap. Bot. 48:242- 276. References NARAYANA,L.L. & D. RAo. 1976. Contributions to the floral anatomy ofHumiriaceae 4. J . Jap. Bot. 51:12- AUIII.E"!',J.B. 1775. Histoire des plantes de Ia Guiane 15. Française 1:564 - 566, 572. NARAYANA,L.L. & D. RAo. 1977. Conrributions to the BAILWJ-;,H. 1874. Histoire des plantes, Série des Houmiri floral anatomy ofHumiriaceae 6. J . Jap. Bot. 52: 145- 5: 51-56. 153. BAR1'H,O.M. & A.E BARIIOSA.1976. Catálogo sistemático OI:rMANN, O. 1971. Pollenmorphologisch systematische do pólen das planras arbóreas do Brasil Meridional Untersuchungen innerhalb der . XXlI - Linaceae, Humirioideae e Erytroxylaceae. Mem. Dissertationes Botanicae 11: 1-163. Inst. Oswaldo Cruz 74:203-212. Or:rMANN, O. 1975a. Linaceae. Palynologica Madagassica BEJ-;1'HAM,G. 1853. Notes on Humiriaceae. Hooker Joum. et Mascarenica. Pollen Spores 17:11-42. Bot. Kew Gard. Misc. 5:97-104. OI.1'MANN, O. 1975b. Erythroxylaceae. Palynologica BEN1'HAM,G. & J.D. Hooker. 1862. Humiriaceae, p. 246- Madagassica et Mascarenica. Pollen Spores 17: 54-57. 247. In: BLACK,A. (Ed.), Genera Plantarum 1. PLANCHON,J. E. 1848. Sur La Famille Des Linnées. Hooker BOVE,c.P. 1996. Palinotaxonomia e filogenia da família Joum. Bot. Kew Gard. Misc. 6:588. 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Orstom 40: 1-40. MAR1'IUS,C.E.P. 1827. Nova genera et especies planrarum YUNUS, D. & P.K.K. NAIR. 1989. Pollen morphology of brasiliensium. Leipzig, Vol.2. Indian Geraniales: A Research Monograph. New ME1'CAI.FE, C.R.; M. LESC01' & D. LOIIREAU. 1968. A propos Delhi, Today's & Tomorrow's Printer & Publishers. de quclques anatoll1iques et palynologiques comparés

24 J. CampoBiol. 2(1) 1997