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This large and well-supported clade is quite unresolved and includes seven campanuloid genera and 11 species of Campanula. Overall, this group can be considered a large paraphyletic Asyneuma, with two early diverging Asyneuma lineages, respective the unresolved A. michauxioides–A. lobelioides–A. virgatum clade, and the monotypic A. trichocalycina clade, and a third group with low support containing remaining accessions of Asyneuma plus other genera. Within the last clade, some particular assemblages are further delimited with confidence, including e.g. a disjunct European/American clade encompassing Legousia, Triodanis, and three species of Campanula, a mostly Iranian clade containing C. acutiloba, C. humillima, C. luristanica, and C. perpusilla, depicted for the first time, or the C. samothracica–C. cretica clade.

Asyneuma is a group of mostly perennial, robust and erect herbs with deeply divided corollas, ranging from SE Europe to E Asia, most of the specific diversity being encountered in the Middle-East (Lammers 2007, Damboldt 1978). While the inclusion of Asyneuma in a paraphyletic Campanula has been long established (Eddie & Ingrouille 1999, Roquet & al. 2008), its polyphyly is suggested here for the first time. Indeed, the most detailed study so far done for that group (Frajman & Schneeweiss 2009), including eight species of Asyneuma, overall supported a monophyletic genus by transferring the problematic A. comosiforme into Campanula.

The geographically disjunct Campanula–Legousia–Triodanis clade shows a paraphyletic genus Legousia with respect to a derived North American clade, overall suggesting a single dispersal to the Americas from a Legousia-like Mediterranean ancestor during the Late Miocene (11,78 Ma [4,71–14,63]). This single introduction was quickly followed by the diversification of several lineages now represented by Campanula (incl. Campanulastrum), and Triodanis. Close relationships between the annual taxa of Legousia (4 species) and Triodanis (6 species) have long been suggested, the two genera being sometimes merged due to the scarcity of segregating morphological differences, including the degree of stem branching or the corolla shape (Shetler & Morin 1986, McVaughn 1945) or some similarities in chromosome numbers (x = 7, 8, and 10 present in both Legousia and Triodanis). Our results largely support and amend recent works (Haberle & al. 2009, Wendling & al. 2011) that inferred a similar Eurasian - American disjunction (but without age estimates), and further show the lability of the respective annual and perennial conditions in the campanuloids. In the present case, the annual condition observed in both Legousia and Triodanis shows reversals to the perennial condition in the rare endemics C. reverchonii of Texas and C. floridana of Florida, or the Eastern North American C. americana. Mediterranean/American disjunct patterns have been exemplified for other plant groups, including the Betoideae, the mostly annual Chironiinae (Gentianaceae), Lithospermum (Boraginaceae), Lotus or Lupinus (Fabaceae) (Allan & Porter 2000, Drummond 2008, Mansion & Struwe 2004, Mansion & Zeltner 2004, Weigend & al. 2009, Hohmann & al. 2006).

Another Eurasian-American pattern can also been observed between a Himalayan Asyneuma argutum clade (two subspecies) and the circumboreal-American Campanula uniflora, the two entities having diverged in the Late Miocene (7.60 Ma [2.64–11.22]. Also weakly supported by the petD reconstruction, the position of C. uniflora into an Asyneuma lineage has been inferred by other studies (Wendling & al. 2011, Frajmann & Schneeweiss 2009).

The strongly supported, mostly Iranian clade C. acutiloba–C. humillima–C. luristanica–C. perpusilla encompasses morphologically similar species, mostly separated by inconspicuous morphological traits (Rechinger & Schiman-Czeika 1965). Indeed, the sister clade C. luristanica–C. humillima denote strong genetic relationships between two species sometimes considered varieties of each other’s. In the same way, the rare C. hermanii, just known from the type locality, is morphologically separated from C. humillima by the presence of sub-succulent leaves, a quite labile character. Overall, the three last-mentioned “species” could represent only one, and reflect potential taxonomic redundancy.

Finally, clade Cam04 contains three Aegean endemics, i>C. cretica, C. samothracica, and Petromarula pinnata. The sister relationships between C. cretica and C. samothracica, sometimes considered as subspecies, are depicted here for the first time. Our data suggest a Miocene origin for this clade (14,24 Ma [8,19–17,02]), followed by a Pleistocene diversification (0,62 Ma [0,02–3,08]), overall suggesting very recent arrival of C. cretica in Crete. Recent studies (Cellinese & al. 2009), only including the Cretan endemic, inferred a putative age of 24 (±10) Ma for the C. cretica lineage, advocating that “this species represents another continental remnant that has not diversified in isolation”. At last, the phylogenetic position of Petromarula, which has been considered a sister lineage to the Phyteuma–Physoplexis clade, but with low support (Cellinese & al. 2009), is unresolved using petD sequences. This genus was first segregated from Phyteuma owing to the unique presence of pinnate leaves, quasi-absence of pollen collector hairs, and a showy club-shaped stigma.

From: Mansion & al. (2012: 11)


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