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Phylogeny, Morphological Evolution, and Speciation of Endemic Brassicaceae Genera in the Cape Flora of Southern Africa Author(S): Klaus Mummenhoff, Ihsan A

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Phylogeny, Morphological Evolution, and Speciation of Endemic Brassicaceae Genera in the Cape Flora of Southern Africa Author(S): Klaus Mummenhoff, Ihsan A Phylogeny, Morphological Evolution, and Speciation of Endemic Brassicaceae Genera in the Cape Flora of Southern Africa Author(s): Klaus Mummenhoff, Ihsan A. Al-Shehbaz, Freek T. Bakker, H. Peter Linder, Andreas Mühlhausen Reviewed work(s): Source: Annals of the Missouri Botanical Garden, Vol. 92, No. 3 (Oct., 2005), pp. 400-424 Published by: Missouri Botanical Garden Press Stable URL: http://www.jstor.org/stable/40035479 . Accessed: 29/02/2012 04:58 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. Missouri Botanical Garden Press is collaborating with JSTOR to digitize, preserve and extend access to Annals of the Missouri Botanical Garden. http://www.jstor.org PHYLOGENY, Klaus Mummenhoff,2 MORPHOLOGICAL Ihsan A. Al-Shehbaz,3 Freeh T. Bakkerf EVOLUTION,AND H. Peter hinderf SPECIATIONOF ENDEMIC and Andreas Miihlhausen6 BRASSICACEAEGENERA IN THE CAPE FLORA OF SOUTHERNAFRICA1 Abstract Heliophila (ca. 73 spp.), the ditypic Cycloptychisand Thlaspeocarpa,and the monotypic Schlechteria, Silicularia, Brachycarpaea, and Chamira are endemic to the Cape region of South Africa, where they are the dominant genera of Brassicaceae. They may be regarded as the most diversified Brassicaceae lineage in every aspect of habit, leaf, flower, and fruit morphology.The characters used in the separation of these genera and their species, especially fruit type (silique vs. silicle), dehiscence (dehiscent vs. indehiscent), compression (latiseptate vs. angustiseptate),and cotyledonary type (spirolobal, diplecolobal, twice conduplicate), have been used extensively in the delimitation of tribes. The rela- tionship and taxonomic limits among these genera are unclear and controversial. The present ITS study demonstrates the monophyly of tribe Heliophileae, with Chamira as sister clade. The other five smaller genera above are nested within two of the three main lineages of Heliophila, to which they should be reduced to synonymy.The current study reveals parallel evolution of fruit characters often used heavily in the traditional classification schemes of the family. However, the arrangementof species into three main clades largely corresponds with the distribution of morphological characters (e.g., habit, leaf shape, seed structure, inflorescence type, and pres- ence/absence of basal appendages on the pedicels, petals, and staminal filaments) not adequately accounted for in previous studies. Estimation of divergence times of the main lineages of Heliophila is in agreement with recent esti- mations in other plant groups, all of which date the diversification against a backgroundof aridificationin the Pliocene and Pleistocene. Species of one main clade are perennial, microphyllous shrubs/subshrubstypically restricted to poor sandstone soils in the southwesternand western parts of the Cape Floristic Region of South Africa. Species of the other two clades are predominantlyannuals that grow in more arid regions of Namibia and Namaqualand,as well as in the above sandstone areas of the Cape Region. The adaptive significance of various floral structures is discussed in terms of their possible role in the rapid diversification within Heliophila. Key words: Brachycarpaea,Cape flora, Cape Floristic Region, Chamira, Cycloptychis,Heliophila, Heliophileae, ITS, phylogeny, radiation, Schlechteria, Silicularia, speciation, Thlaspeocarpa,trnL-F. Seven genera of Brassicaceae, Heliophila (73 represent the dominant Brassicaceae. Although spp.), Cycloptychis(2 spp.), Schlechteria (1 sp.), Si- several classification systems (Table 1) have been licularia (1 sp.), Thlaspeocarpa (2 spp.), Brachy- proposed (e.g., Hayek, 1911; Schulz, 1936; Jan- carpaea (1 sp.), and Chamira (1 sp.), are endemic chen, 1942), the relationships among these genera to southern Africa (for authornames of these genera remain unresolved. In a recent re-evaluation of the and their species, see Table 1 and Appendix 1). group, Appel and Al-Shehbaz (1997) placed the Most species occur in the winter-rainfallarea of the first six genera in the tribe Heliophileae and re- western Cape Floristic Region (CFR), where they tained Chamira in the monotypic Chamireae.They 1 We are grateful to the directors, curators, and collectors of the institutions that provided the plant material. We thank Ulrike Coja for technical assistance, Andreas Franzke for fruitful discussions, and Adelaide Stork, Ashley Nicholas, and two anonymous reviewers for constructive criticisms that helped improve the final draft. 2 Departmentof Botany, Faculty of Biology/Chemistry,University of Osnabrtick,Barbarastrasse 11, 49069 Osnabriick, [email protected]. 3 Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri, U.S.A. 63166-0299. 4 [email protected]. National Herbarium Nederland, Wageningen branch & Biosystematics Group, Wageningen University, Generaal Foulkesweg 37, 6703 BL Wageningen,The Netherlands, [email protected]. 5 Institute of Systematic Botany, University of Zurich, Zollikerstrasse 107, CH-8008, Switzerland, plin- [email protected]. 6 Departmentof Botany,Faculty of Biology/Chemistry,University of Osnabriick,Barbarastrasse 11, 49069 Osnabriick, [email protected]. Ann. Missouri Bot. Gard. 92: 400-424. Published on 10 October 2005. Volume 92, Number 3 Mummenhoff et al. 401 2005 Brassicaceae In Cape Flora 0^ C^ & 02 02 QJ characterized the by dipleco- 2 cd cd cd cd cd cd Heliophileae having lobal cotyledons (elongated and twice transversely folded). This uncommon cotyledonary type is also ill " ' j!!!!!l <J ^ ^ ^3 ro3^a3 13 ^ ^3 known in three Australian species of Lepidium L. sect. Monoploca (Bunge) Prantl subsect. Diploploca Hewson (Hewson, 1981; Mummenhoffet al., 2001), I making this character homoplastic. '53 §• The Heliophileae may be regarded as the most cd diversified Brassicaceae lineage in every aspect of habit, flower, and fruit morphology (Table 2; com- If I piled from Appel & Al-Shehbaz, 1997). It has flow- C/3 O- cd cd cd i g J9 _2 JH CD CD ers with enormous diversity in size rangingfrom the mill largest in the family (petals to 25 mm long in Bra- _fi CD CD CD a; 3 I chycarpaea juncea and Cycloptychis virgata) to CJ ffi ffi ffi J J I nearly the smallest (petals ca. 1.2 mm long in He- liophila pectinata). Heliophila has a wide range of flower color, including blue, a color otherwise 1 known in Brassicaceae only in the unrelated Hi- malayan Solms-laubachia Muschl. (Al-Shehbaz & %% % % the flowers have 1.2 t§Cd C^ CD CD CD CD CD j| Yang, 2001). Furthermore, usually on the basal of and/or o .h a a a a « appendages portions petals . Several H. Mg | .2 £ £ £ g staminal filaments. species (e.g., afri- ^ 13 13 T3 13 j^ I ffi ffi K ffi < beaked fruits similar to those of the | u I cana) produce g tribe Brassiceae, whereas others have siliques more ^ id v m iu than 12 cm long (e.g., H. scoparia) or minute sili- cles only about 2 mm in diameter (e.g., H. patens). T 11111 Fruit shape is quite variable (linear, lanceolate, ob- -J^ S 2 .2 .2 .2 or whereas fruit com- r| ^_^ j^ f CD CD U long, elliptic, ovoid, globose), in varies from Q ^S i i i i i pression Heliophila latiseptate (flat- l^q] "-rH ' cd cd cd cd cd tened to the to and in cd 2 .2 .2 .2 .2 parallel septum) terete, sa3 ^a '*& a'"B a '*B a '^B a Brachycarpaeait is angustiseptate (fruitflattened at ^ ^r*^ ^r*Js* Js* a to the 1, Fruits CD CD CD CD CD CD right angle septum) (Figs. 2). may | £££££ | | be dehiscent (Heliophila), indehiscent and woody J (Silicularia), samaroid (Thlaspeocarpa), or even and with a distinct or cd cd schizocarpic (Cycloptychis) rt cd pf| CD CD rudimentary carpophore (Brachycarpaea). These O CD ^O CD *S fruit characters (e.g., silique versus silicle, dehis- 1 IS |l cent vs. indehiscent, latiseptate vs. angustiseptate), 1 a£ which are used in the separation of species and genera within Heliophileae, have been used exten- sively in the delimitation of tribes (see Al-Shehbaz, 1984). Within Heliophila one finds ephemeral to perennial herbs, shrubs, and lianas to 3 m tall (H. I scandens). Apart from previous controversial clas- ! Pi! sification discussed and Al-Sheh- S ffi ffi I I M I systems by Appel "S3_CD baz (1997), nothing is known about the phyloge- >» CO netic relationships within the Heliophileae. The most striking features of the CFR are the I I high level of endemism and the remarkablespecies richness. estimated at about 9000 J ^» Species richness, "Sq-§| species in an area of 90,000 km2(Goldblatt & Man- ning, 2000), is comparable to those of the most di- verse equatorial areas, and species endemism of ca. I Illllii 70% is similar to that found on islands (Linder, 2003). In a recent review on the origin of the Cape 402 Annals of the Missouri Botanical Garden 8 % I I e ° ^ « g 22 £ jb * a>1fa = * i i li mil ifi I ^ r-H cc cdcfi(Na3Oa3T3a3OH^t« bO cdcc i ., ,«ii ii.j -i g 4 IlslllillJlU II fill- -siiS ti i j ! I !i iililiri I |I I I I I i!:Ii!!n-H g il I I s I 1 ^ ° | ^ I 15 lie "f 11 I I I .-S-i bIS I .1 -S3 I I 1!!^o!ii! ^1^ b§o| S S - ^ P S ^ " 6 | -8 ^ £ = *« I lilllj if I ?9 ^ 11 BiJiillfJJ I" If Volume 92, Number 3 Mummenhoff et al. 403 2005 Brassicaceae in Cape Flora Figure 1. Strict consensus ITS tree with the distribution of morphological data in Heliophila and related genera. Cleome spinosa (Cleomaceae), Aethionema saxatile, Alliaria petiolata, Rorippa amphibia, and Cardamine matthioli (Brassicaceae) served as the outgroup.
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