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Delimitation of Malagasy Tribe Coleeae and Implications for Fruit Evolution in Bignoniaceae Inferred from a Chloroplast DNA Phylogeny

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Delimitation of Malagasy Tribe Coleeae and Implications for Fruit Evolution in Bignoniaceae Inferred from a Chloroplast DNA Phylogeny Plant Syst. Evol. 245: 55–67 (2004) DOI 10.1007/s00606-003-0025-y Delimitation of Malagasy tribe Coleeae and implications for fruit evolution in Bignoniaceae inferred from a chloroplast DNA phylogeny M. L. Zjhra1, K. J. Sytsma2, and R. G. Olmstead3 1Department of Biology, Georgia Southern University, Statesboro, GA, USA 2Department of Botany, University of Wisconsin, Madison, WI, USA 3Department of Botany, University of Washington, Seattle, WA, USA Received February 2, 2003; accepted April 23, 2003 Published online: February 23, 2004 Ó Springer-Verlag 2004 Abstract. Coleeae (Bignoniaceae) are a tribe almost the Gondwanan continent, Madagascar was entirely restricted to Madagascar. Coleeae have attached to Africa at present day Somalia, previously been placed in neotropical Crescentieae Kenya and Tanzania until 165 mya (Rabino- due to species with indehiscent fruits, a character witz et al. 1982, 1983). Madagascar was otherwise unusual in Bignoniaceae. A phylogeny completely separated from Africa by ndh trn based on three chloroplast regions ( F, T-L 120 mya (Rabinowitz et al. 1983), but spacer, trnL-F spacer) identifies a monophyletic remained attached to India until 88 mya Coleeae that is endemic to Madagascar and sur- rounding islands of the Indian Ocean (Seychelles, (Storey et al. 1995). During the lower Creta- Comores and Mascarenes). African Kigelia is not a ceous Madagascar traveled to its present member of Coleeae, rather it is more closely related position 400 km off the coast of Mozambique to a subset of African and Southeast Asian species (Fig. 1). The granitic islands of the Seychelles, of Tecomeae. The molecular phylogeny indicates in the Indian Ocean north of Madagascar, that indehiscent fruit have arisen repeatedly in represent fragments of the separation of Mad- Bignoniaceae: in Coleeae, Kigelia and Crescentieae. agascar-India from Africa. In reference to The characteristic fleshy fruits of species of Coleeae Madagascar, Wallace (1895) remarked: ‘‘there likely arose autochthonously in Madagascar. Within is probably no portion of the globe that Coleeae Colea and Ophiocolea are sisters, Phyllar- contains within itself so many and such varied thron Colea Ophiocolea Rho- is sister to + ,and features of interest connected with geograph- docolea is sister to the rest of the tribe. ical distribution.’’ A few taxa of Madagascar’s Key words: Bignoniaceae, biogeography, Coleeae, flora may reflect the original Gondwanan flora Crescentieae, fruit evolution, Kigelia, Madagascar, such as gymnosperms and the phylogenetically ndhF, phylogenetics, trnT-L spacer, trnL-F spacer. basal angiosperms Takhtajania (Winteraceae) (Karol et al. 2000) and Ascarinopsis (Chlo- The large island of Madagascar is in many ranthaceae). The majority of Madagascar’s respects a micro-continent. Originally part of flora has likely arrived via dispersal, either 56 M. L. Zjhra et al.: Phylogenetics of Coleeae Fig. 1. Origin of indehiscent fruits in Bignoniaceae according to Gentry (1976). Crescentieae were hypothesized to have been derived from neotropical Tecomeae, with mammal-dispersed, indehiscent fruits evolving from dehiscent fruits. In contrast, Coleeae were derived from Malagasy/African Tecomeae, with baboon- and lemur-dispersal evolving from wind dispersal. Shading indicates distribution of tropical species of Tecomeae long-distance or by way of (now under water) tinent. An additional 16 Malagasy species of oceanic ‘‘stepping stone’’ islands (Gentry 1988, Bignoniaceae belong to tribe Tecomeae. Spe- Schatz 1996). In this respect, Madagascar is cies of Malagasy Coleeae are concentrated in like an oceanic island whereby the majority of the tropical rainforests of Madagascar, with the flora originates via long-distance dispersal. peripheral distribution in Madagascar’s wes- Radiations in species number and/or ecologi- tern dry deciduous forests and the arid spiny cal adaptations such as pollination biology, scrub of the south. Five genera of Malagasy fruit dispersal, and leaf type are common in Coleeae (Rhodocolea, Ophiocolea, Colea, these isolated groups (e.g. Coleeae, Bignonia- Phyllarthron, and Phylloctenium) have been ceae [Gentry 1988]; Adansonia, Bombacaceae delimited on the basis of fruit, flower, and [Baum 1995, Baum et al. 1998]; Dalechampia, leaf characteristics (Perrier de la Baˆ thie Euphorbiaceae [Armbruster et al. 1993]; Didi- 1938a, b). According to Gentry (1976), Rho- ereaceae [Applequist and Wallace 2000]). docolea retains primitive characteristics; after Among biogeographic areas, Madagascar the derivation of Rhodocolea, two lineages of has the second richest flora of Bignoniaceae, more specialized taxa evolved: Ophiocolea/ following South America. The majority of Colea, and Phyllarthron/Phylloctenium. Oph- Malagasy species of Bignoniaceae belong to iocolea gave rise to Colea, and Phyllarthron tribe Coleeae, a group that has been tradi- gave rise to Phylloctenium (Gentry 1976). tionally delimited to include 49 species, of The mostly endemic Malagasy Coleeae which 44 are endemic to Madagascar and are of considerable, and sometimes conten- four to the islands of the Indian Ocean (the tious, evolutionary, biogeographic and sys- Seychelles, Comores, and Mascarenes), and tematic interest. Much of the taxonomic one (monotypic Kigelia) to the African con- history of Coleeae relates to the evolution M. L. Zjhra et al.: Phylogenetics of Coleeae 57 of indehiscent fruits in Bignoniaceae. Species indehiscent fruits with subsequent modifica- of tribe Coleeae are remarkable for their tion in related lineages back to dehiscent diversity of fleshy fruits (in a family charac- fruits with wind dispersed seeds. terized by dehiscent fruits), numerous cauli- Further complicating the phylogenetic florous species, variety of pollination and evolutionary picture of the Malagasy syndromes, diversity of habitats occupied, Coleeae is African Kigelia africana. When and high levels of locally endemic, sympatric Gentry (1976) split Crescentieae and Coleeae, species (Zjhra 1998). Originally, taxa now he placed the monotypic Kigelia in Coleeae. comprising the Coleeae were placed in tribe Kigelia is found throughout the savannas and Crescentieae (de Candolle 1838, 1845; See- gallery forests of Central Africa. Its meter- mann 1860; Baillon 1887, 1888; Perrier de la long, pendulous, baboon-dispersed fruits Bathie 1938a, b), an otherwise neotropical have inspired much folklore and earned it group distributed primarily in Central Amer- the moniker, Sausage Tree. Kigelia shares ica and the Caribbean. The geographically geographic proximity with Coleeae, and disjunct Crescentieae and Coleeae share a unusually large indehiscent fruits and bat number of characteristics otherwise not ob- pollination with Crescentieae. The placement served in the family: spines, phyllodes, simple of Kigelia is important in formulating phylo- leaves, cauliflory, and fleshy indehiscent genetic and biogeographic hypotheses regard- fruits. Gentry (1976) suggested that Crescen- ing the origins of Coleeae, as well as tieae were derived from neotropical Teco- assessment of the phylogenetic status (i.e. meae, with mammal-dispersed, indehiscent homoplasy or homology) of the characters fruits evolving from dehiscent fruits with that appear to be synapomorphic for Coleeae wind dispersed seeds. Coleeae were hypothe- and Crescentieae. sized by Gentry (1976) to have been derived These important systematic, biogeograph- from Malagasy/African Tecomeae, with ba- ic, and evolutionary questions require an boon and lemur dispersal evolving from wind independent, molecular-based phylogenetic dispersal (Fig. 1). Leroy (1978) suggested that framework for their resolution. Only one Malagasy ‘‘Crescentieae’’ originated during previous molecular study has attempted to post-Gondwanan time, and evolved from examine relationships within Bignoniaceae. ancestors (now extinct) common to Africa Spangler and Olmstead (1999), using rbcL and South America. Gentry (1976, 1988) and ndhF sequence variation of 19 genera of argued on the basis of geographic disjunction Bignoniaceae, indicated that Kigelia and that species of Coleeae and Crescentieae Ophiocolea (the only sampled genera of shared similar features due to convergent Coleeae) were sister taxa and related to a evolution rather than common ancestry. complex of Old World and New World Combining Crescentieae and Coleeae as a representatives of Tecomeae and Crescen- single tribe (following de Candolle 1838, tieae. The molecular phylogenetic analysis 1845; Seemann 1860; Baillon 1887, 1888; presented here increases taxon sampling of Perrier de la Baˆ thie 1938a, b) results in a the Malagasy tribe Coleeae and other pre- remarkable disjunct distribution that must be sumed relatives in Bignoniaceae and aims to explained either by long-distance dispersal assess (1) the phylogenetic status of Coleeae, between South America and Madagascar, or in particular its relationship with Crescentieae by complete extinction of all representatives and Kigelia; (2) the evolution of morpholog- of a once more widespread Crescentieae/ ical traits (indehiscent fruits, spines, phyll- Coleeae lineage in Africa, south Asia, and odes) that have variously united and South America. Separating Crescentieae and separated Coleeae, Crescentieae, and Kigelia; Coleeae requires either convergent evolution and (3) the relationships of genera within of indehiscent fruits, or a single origin of Coleeae. Table 1. Accessions of Coleeae and outgroups for which sequences were included in phylogenetic analyses. Numbers represent
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