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Correlations Among Fruit Traits and Evolution of Different Fruits Within

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Correlations Among Fruit Traits and Evolution of Different Fruits Within BolankdJournul oJ/h Linnean Sociplv (20OO), I.?.?: 303-326. With G figures doi:l0.lOOS/lmjl. 1999.0340, available online at http://www.idealibrary.rom on I hi" Correlations among hittraits and evolution of different hits within Melastomataceae GUDRUN CLAUSING'*, KARSTEN MEYER' AND SUSANNE S. RENNER' 'Institut$r Spezielh Botanik, Universitat Main<, 0-55099 Main< Germany, 'Department of Biology, Universip of Missouri-St. Louis, 8001 Natural Bridge Rd., St. Louis, M063121- 4499, us;4 RecciwdJu~1999; accepted for publicdwn Februaty 2000 The anatomy and morphology of nearly mature fruits in 85 mainly palaeotropical species of Melastomataceae were examined using microtome- and hand-sectioning, and differential staining. Much structural heterogeneity was observed in both capsules and berries. Mul- tivariate analyses of 31 of the 52 characters recorded for each species, revealed that indehiscence is associated with fusion of ovary and hypanthium tissues, placenta persistence, lack of a persistent endocarp, and a dearth of srlereids in these tissues, while dehiscenre is correlated with the opposite states and a persistent exocarp. Other fruit characters such as lignification or fleshiness of tissues do not show a consistent association with dehiscence. Break down of broad fruit types, such as 'berry' and 'capsule', into their individual morphological and anatomical traits shows how unusual fruit types, such as woody berries, fleshy capsules, and capsules containing fleshy placentas (display fruits), which are common in palaeotropical Melastomeae and Dissochaeteae, contribute to a loosening of expected correlations. Thus, discriminant analysis clearly differentiated display fruits from the other fruit types because of their combination of fleshy placentas with a persistent endocarp and absence of ovary/hypanthium fusion. The evolution of fruit types within Melastomataceae, and especially Dissochaeteae, and their reliability as phylogenetic indicators is discussed in the light of molecular phylogenies for these groups that show that berries and capsules evolved several times independently, explaining the observed heterogeneity of outwardly similar fruits. Fruit diversity within Melnrtoma, a monophyletic genus of 22 species, provides an example of the plasticity afforded by the particular construction of Melastomataceae fruits, which has contributed to ecological diversification in melastome seed dispersal. 0 2000 The Linnean Society of London ADDITIONAL KEY WORDS:-berries ~ capsules ~ dispersal mechanisms - display fruits - Dissochaeteae - multivariate analysis - phylogeny. CONTENTS Introduction. ...................... 304 Material and methods ................... 305 Results ........................ 308 General anatomy and morphology of melastome fruits ....... 308 * Corresponding author. E-mail: [email protected] 303 OO2&4O74/OO/07O303 + 24 $35.00/0 0 2000 The IdinnranSociety of London 304 G. CLAUSING ETA. Characters and their states ................ 310 Multivariate analyses .................. 312 Discussion ....................... 314 Structural heterogeneity of berries and capsules .......... 314 Fruit evolution in Melastomataceae, especially in the Dissochaeteae/Sonerileae complex ............. 316 Fruit variation at the intrageneric level: the case of Melastoma ..... 319 Fruit types as phylogenetic indicators ........ ..... 320 Fruit character plasticity and dispersal ecology .......... 320 Acknowledgements .................... 321 References .................. ..... 322 INTRODUCTION Fruit types such as capsule, nut, drupe, samara and berry have sometimes been regarded as evolutionarily conservative (Stebbins, 1974; Spjut, 1994); indeed, many older classification systems accorded fruit type a high taxonomic weight. However, molecular phylogenetic studies are showing that fruits often are unreliable indicators of natural alliances and that their use in higher-level classification has created artificial groups (Apiaceae: Plunkett, Soltis & Soltis (1996); Lamiales d.:Wagstaff & Olmstead (1997); Myrtaceae: Johnson & Briggs (1 984); Ranunculaceae: Hoot (1995); Rhamnaceae: Richardson & Medan (pers. corn., Sept. 1997); Rosaceae: Rohrer, Robertson & Phipps (1991), Morgan, Soltis & Robertson (1994); Saxi- fragaceae: Soltis, Soltis & Bothel (1990)).In Rubiaceae, for example, tracing of fruit evolution on a molecular phylogenetic tree suggests that fleshy fruits have evolved 12 times independently within that family (Bremer & Eriksson, 1992; Bremer, Andreasen & Olsson, 1995). Moreover, molecular data are showing that fruit evolution may be rapid when morphogenetic genes of major effect are involved that can cause dramatic morphological differences (cf. Kadereit , 1994). The striking homoplasy of fruit types may have two causes. First, it may result from strong directional selection on fruit characters; the latter are highly adaptive and directly correlated with the dispersal agent. For example, fleshy fruits normally are associated with dissemination by animals. Second, fruit characters may appear more homoplastic than they really are because of incorrect homology assessments. This is a problem particularly in large tropical families, such as Rubiaceae and Melastomataceae, where detailed morphological and anatomical studies based on appropriately preserved material are scarce (but see Igersheim, 1993; Rohwer, 1996). Here we investigate the morphological and anatomical plasticity of fruits in Melastomataceae. Melastomataceae are part of Myrtales, which include families with both dry and fleshy fruits. Examples are Myrtaceae (capsules, nuts, drupes, and berries), Lythraceae s.1. (capsules and berries), Onagraceae (capsules, nuts, berries), and Melastomataceae (capsules, berries, and several intermediate types). Johnson and Briggs ( 1984) concluded from their morphology-based phylogenetic study of Myrtaceae that the traditional three subfamilies delimited by succulent and indehiscent versus dry and dehiscent fruits had to be abandoned since fleshiness of the ovary, and fleshiness of both ovary and hypanthium, each arose independently at least twice. In Lythraceae, berries of Sonneratiu and rZlnicu evolved independently (Graham, Crisci & Hoch, 1993), and in Onagraceae, the nut-like fmits of Heterguuru originated from ancestors that had septicidal Clarh-type capsules (Sytsma & Gottlieb, 1986). FRUIT TRAITS IN MEIASTOMATACEAE 305 These examples from close relatives of the Melastomataceae (Conti, Litt & Sytsma, 1996) suggest that phylogenetic investigations, followed by critical morphological homology assessments, are needed if fruit characters are to be used in phylogenetic analyses of this family. Tribal classifications of Melastomataceae (De Candolle, 1828; Naudin, 1851; Triana, 1871; Cogniaux, 1891; Renner, 1993) have relied heavily on fruit types, both as diagnostic characters as well as supposed phylogenetic markers (Renner, 1993). Based on outgroup comparison, Renner considered dry capsules as plesiomorphic for the family and fleshy fruits from inferior ovaries with seeds embedded in pulp (her ‘true berries’) as apomorphic. Because she was aware of the plasticity of fruit characters, especially the different origins of fleshy fruit walls and modes of dehiscence, she used only one fruit character in her analysis, namely the presence and absence of true berries, suggesting that further critical examination of fruit attributes was needed (Renner, 1993: 529). The present study examines the fruit anatomy and morphology of 85 species of Melastomataceae, representing the mainly palaeotropical Astronieae, Dissochaeteae, Kibessieae, Melastomeae, and Sonerileae, and a few neotropical Blakeeae, Me- lastomeae, Miconieae, and Bertolonieae (for tribal classification, see Material and methods). Our major goal was to investigate whether the terms capsule and berry as traditionally applied in these groups describe structurally homogeneous phenotypes. To this end we performed multivariate analyses of 31 anatomical and morphological characters to identifjr states that might correlate with fruit dehiscence (or a lack thereof). We also investigated the pattern of plasticity of fruit characters at different hierarchical levels and within monophyletic groups, as identified by molecular sequence data, and tried to relate it to ecological determinants. MATERIAL AND METHODS Fruits of 85 species of Melastomataceae, representing 3 1 genera and eight tribes were investigated (see Appendix in which we follow the classification of Renner (1 993); we recognize Bertolonieae and Dissochaeteae semu Cogniaux (189 1) based on molecular phylogenetic results (Clausing, 1999; Clausing & Renner, in press), although the circumscription of these tribes at present is unclear). Fruits came from alcohol samples (70 spp.) collected in South-east Asia, Madagascar, and South America, from herbarium specimens (7 spp.), or from plants cultivated at the Botanical Garden Mainz (8 spp.). We analysed nearly mature fruits. Cross-sections of fruits of ten species were made using a microtome and then stained with toluodine blue, which stains cell walls; the remaining material was hand-sectioned. Herbarium material was boiled prior to sectioning. Manual sections were stained with phloroglucine+ HC1 or with iodine in potassium iodide solution, staining lignin and starch, respectively. They were preserved in Hoyer’s solution (Kearns & Inouye, 1993), which bleaches tissue, bringing out lignified cells and mineral crystals. Fifty-two characters were coded in binary fashion (Table 1) and
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