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Phylogeny and Biogeography of Isophyllous Species of Campanula (Campanulaceae) in the Mediterranean Area

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Phylogeny and Biogeography of Isophyllous Species of Campanula (Campanulaceae) in the Mediterranean Area Systematic Botany (2006), 31(4): pp. 862–880 # Copyright 2006 by the American Society of Plant Taxonomists Phylogeny and Biogeography of Isophyllous Species of Campanula (Campanulaceae) in the Mediterranean Area JEONG-MI PARK,1 SANJA KOVACˇ IC´ ,2 ZLATKO LIBER,2 WILLIAM M. M. EDDIE,3 and GERALD M. SCHNEEWEISS4,5 1Department of Systematic and Evolutionary Botany, Institute of Botany, University of Vienna, Rennweg 14, A-1030 Vienna, Austria; 2Botanical Department and Botanical Garden of the Faculty of Science, University of Zagreb, HR-10000 Zagreb, Croatia; 3Office of Lifelong Learning, University of Edinburgh, 11 Buccleuch Place, Edinburgh, EH8 9LW, Scotland, U.K.; 4Department of Biogeography and Botanical Garden, Institute of Botany, University of Vienna, Rennweg 14, A-1030 Vienna, Austria 5Author for correspondence ([email protected]) Communicating Editor: Thomas G. Lammers ABSTRACT. Sequence data from the nuclear internal transcribed spacer (ITS) were used to infer phylogenetic relationships within a morphologically, karyologically, and geographically well-defined group of species of Campanula (Campanulaceae), the Isophylla group. Although belonging to the same clade within the highly paraphyletic Campanula, the Rapunculus clade, members of the Isophylla group do not form a monophyletic group but fall into three separate clades: (i) C. elatines and C. elatinoides in the Alps; (ii) C. fragilis s.l. and C. isophylla with an amphi-Tyrrhenian distribution; and (iii) the garganica clade with an amphi-Adriatic distribution, comprised of C. fenestrellata s.l., C. garganica s.l., C. portenschlagiana, C. poscharskyana, and C. reatina. Taxa currently classified as subspecies of C. garganica (garganica, cephallenica, acarnanica) and C. fenestrellata subsp. debarensis are suggested to be best considered separate species. The molecular dating analysis, although hampered by the lack of fossil evidence, provides age estimates that are consistent with the hypothesis that the diversification within the garganica clade was contemporaneous with the climatic oscillations and corresponding sea-level changes during the late Pliocene and Pleistocene. Dispersal-vicariance analysis suggests that the garganica clade originated east of the Adriatic Sea, from where it reached the Apennine Peninsula. KEYWORDS: amphi-adriatic distribution, dispersal-vicariance analysis, molecular dating, taxonomy. Campanula L. is the largest genus within the trum, Legousia Durand, Phyteuma, and others; and Campanulaceae and comprises ca. 300 species (3) a small unnamed third clade, which addition- distributed mainly in extra-tropical areas of the ally includes Gadellia Schulkina and Musschia Dum. northern hemisphere (Meusel and Ja¨ger 1992; The relationships among these three clades and to Shulkina et al. 2003). A major center of species the genus Jasione L. are unresolved. diversity is found in the Mediterranean region, The taxonomic complexity at the generic level where ca. 250 species occur (Geslot in Greuter et al. also occurs, not only at the infrageneric level 1984). Many of those are edaphically and micro- within Campanula s. str. (e.g., the generic recogni- climatically specialized chasmophytes, and as such tion of taxa such as subgenus Roucela (Dumort.) are often narrowly distributed endemics (Dam- Damboldt), but also at the sectional and subsec- boldt 1965b; Kovanda 1970a; Pignatti 1982). tional level. Many authors during the last two The delimitation of Campanula is quite unclear, centuries tried to develop a workable classification and the genus appears to be residual after the of this large genus (e.g., de Candolle 1830; Boissier exclusion of morphologically well-characterized, 1875; Nyman 1878–1882; Janchen 1958; Gadella mainly monotypic, groups as separate genera. 1964, 1966a,b; Contandriopoulos 1984; Kolakovsky Recent molecular phylogenetic studies (Eddie et 1994) but none of these systems seems to be al. 2003) have shown that genera such as Azorina successfully predictive of phylogenetic relation- Feer, Campanulastrum Small, Edraianthus DC., and ships. In addition, taxonomic systems have been Phyteuma L. nest within Campanula. Campanula, erected on the basis of geographically limited including well-marked segregates, groups in three floristic studies, such as the Flora SSSR (Fedorov major clades: (1) the Campanula s. str. clade, which 1957) or Flora of Turkey (Damboldt 1978), and are additionally includes Azorina, Edraianthus, Trache- thus difficult to apply to Campanula of other lium Tourn. ex L. and others; (2) the Rapunculus regions (e.g., Witasek 1906; Hruby 1930, 1934; clade, which additionally includes Adenophora Podlech 1965; Damboldt 1965b; Kovanda 1970b, Fisch., Asyneuma Griseb. & Schenk, Campanulas- 1977; Kovanda and Ancˇev 1989). Such classifica- 862 2006] PARK ET AL.: PHYLOGENY OF ISOPHYLLOUS CAMPANULA 863 FIG. 1. Distribution areas of isophyllous Campanula species in the central Mediterranean area (following Damboldt 1965b; Lovasˇen-Eberhardt and Trinajstic´ 1978; Pignatti 1982; Surina in Kovacˇic´ and Surina 2005). tions were based on morphological characters mostly allopatric and confined to small, often partly refined by karyological data, but the compact areas (Fig. 1). evolution of the morphological and karyological The Isophylla group is further divided by Dam- characters and possible problems with homoplasy boldt (1965b) into a Tyrrhenian ‘‘fragilis group’’ (i.e., are poorly understood in the Campanulaceae as C. fragilis aggr. of Geslot in Greuter et al. 1984: C. a whole. A sound molecular phylogenetic hypoth- fragilis subsp. fragilis and subsp. cavolinii [together esis would address these questions and could C. fragilis s.l.], C. isophylla) and a predominantly eventually aid the construction of a more pre- peri-Adriatic ‘‘garganica group’’ (i.e., C. elatines aggr. dictive taxonomic classification. of Geslot in Greuter et al. 1984: C. fenestrellata subsp. Despite these problems, some smaller groups fenestrellata, subsp. istriaca and subsp. debarensis within Campanula are well-characterized morpho- [together C. fenestrellata s.l.], C. garganica subsp. logically, karyologically, and biogeographically, garganica, subsp. acarnanica and subsp. cephallenica suggesting that they may be monophyletic (e.g., [together C. garganica s.l.], C. elatines, C. elatinoides, C. Carlstro¨m 1986; Runemark and Phitos 1996; Eddie portenschlagiana, C. poscharskyana,andC. reatina; and Ingrouille 1999; Oganesian 2001; Sa´ez and Table 1). This split is supported by the presence of Aldasoro 2003). One of those, hereafter called the two different chromosome numbers, 2n 5 32 in the Isophylla group, comprises European species char- ‘‘fragilis group’’ and 2n 5 34 in the ‘‘garganica acterized by isophylly, long petiolate basal leaves group.’’ Trinajstic´ (in Lovasˇen-Eberhardt and Tri- with kidney-shaped to cordate blades, distinctly najstic´ 1978) recognizes these groups as series petiolate cauline leaves with cordate to ovate Fragiles Trin. and Garganicae Trin., respectively. blades, calyces without appendages between the Additionally, on the basis of leaf hairiness and lobes, erect capsules with basal pores (rarely with pollen size he separates C. elatines and C. elatinoides irregular splits), and orbicular to ovate seeds with from the ‘‘garganica group’’ (sensu Damboldt 1965b) narrowly ridged testa (Damboldt 1965b). This as separate series Elatines Trin. (Table 1), rendering group has a highly fragmented distribution in the series Garganicae exclusively amphi-adriatic in central Mediterranean region, and its species are distribution (Fig. 1). 864 SYSTEMATIC BOTANY [Volume 31 TABLE 1. Classification of the Isophylla group sensu Damboldt (1965b). aTreated as separate species in the main text of Damboldt (1965b), but reduced to subspecies in a ‘‘note added in proof’’ (Damboldt 1965b: 358). Damboldt (1965b) Lovasˇen-Eberhardt and Trinajstic´ (1978) This study fragilis-‘‘Gruppe’’ (group) Campanula sect. Campanula subsect. fragilis clade Elatines (Wohlfarth) Trinajstic´ ser. Fragiles Trinajstic´ C. fragilis Cyrillo C. fragilis Cyrillo C. fragilis Cyrillo C. fragilis subsp. fragilis C. fragilis subsp. fragilis C. fragilis subsp. cavolinii (Tenore) C. fragilis subsp. cavolinii (Tenore) Damboldt Damboldt C. isophylla Moretti [not treated] C. isophylla Moretti garganica-‘‘Gruppe’’ (group) – – – Campanula sect. Campanula subsect. elatines clade Elatines (Wohlfarth) Trinajstic´ ser. Elatines C. elatines Linne´ C. elatines Linne´ C. elatines Linne´ C. elatinoides Moretti [not treated] C. elatinoides Moretti – Campanula sect. Campanula subsect. garganica clade Elatines (Wohlfarth) Trinajstic´ ser. Garganicae Trinajstic´ C. portenschlagiana Roemer & Schultes C. portenschlagiana Roemer & Schultes C. portenschlagiana Roemer & Schultes C. poscharskyana Degen C. poscharskyana Degen C. poscharskyana Degen ‘‘Sammelart’’ (species aggregate) C. garganica Tenore C. garganica subsp. acarnanica [not treated] C. acarnanica Damboldt (Damboldt) Damboldta C. garganica subsp. cephallenica [not treated] C. cephallenica Feer (Feer) Hayeka C. garganica subsp. garganica C. garganica Tenore C. garganica Tenore ‘‘Sammelart’’ (species aggregate) C. fenestrellata Feer C. fenestrellata subsp. debarensis C. debarensis Rechinger f. C. debarensis Rechinger f. (Rechinger f.) Damboldta C. fenestrellata subsp. fenestrellata C. fenestrellata Feer [s. str.] C. fenestrellata subsp. fenestrellata C. fenestrellata subsp. istriaca (Feer) C. istriaca Feer C. fenestrellata subsp. istriaca Damboldt
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