Cam04
Content
Systematics
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)
Allan G.J. & Porter J.M. 2000: Tribal delimitation and phylogenetic relationships of Lotea and Coronilleae (Faboideae: Fabaceae) with special reference to Lotus: evidence from nuclear ribosomal ITS sequences. – Amer. J. Bot.87: 1871–1881 .
Cellinese N., Smith S.A., Edwards E..J, Kim S.T., Haberle R.C., & al. 2009: Historical biogeography of the endemic Campanulaceae of Crete. – J. Biogeogr.36: 1253–1269 .
Damboldt J. 1978: Campanulaceae – Pp. 2–65 in: Davis PH., (ed.), Flora of Turkey and the East Aegean Islands. – Edinburgh: University Press.
Drummond C.S. 2008: Diversification of Lupinus (Leguminosae) in the western New World: Derived evolution of perennial life history and colonization of montane habitats. – Mol. Phylogenet. Evol.48: 408–421 .
Eddie W.M.M. & Ingrouille M.J. 1999: Polymorphism in the Aegean “five-loculed” species of the genus Campanula, Section Quinqueloculares (Campanulaceae). – Nord. J. Bot.19: 153–169 .
Frajman B. & Schneeweiss G.M. 2009: A Campanulaceous Fate: The Albanian Stenoendemic Asyneuma comosiforme in Fact Belongs to Isophyllous Campanula. – Syst. Bot.34: 595–601 .
Haberle R.C., Dang A., Lee T., Penaflor C., Cortes-Burns H., & al. 2009: Taxonomic and biogeographic implications of a phylogenetic analysis of the Campanulaceae based on three chloroplast genes. – Taxon58: 715–734 .
Hohmann S., Kadereit J.W. & Kadereit G. 2006: Understanding Mediterranean-Californian disjunctions: Molecular evidence from Chenopodiaceae-Betoideae. – Taxon55: 67–78 .
Lammers T.G. 2007: World checklist and bibliography of Campanulaceae. – Kew: Royal Botanical Garden. 675 p.
Mansion G. & Struwe L. 2004: Generic delimitation and phylogenetic relationships within the subtribe Chironiinae (Chironieae : Gentianaceae), with special reference to Centaurium: evidence from nrDNA and cpDNA sequences. – Mol. Phylogenet. Evol.32: 951–977 .
Mansion G. & Zeltner L. 2004: Phylogenetic relationships within the new world endemic Zeltnera (Gentianaceae-Chironiinae) inferred from molecular and karyological data. – Amer. J. Bot.91: 2069–2086 .
Mansion G., Parolly G., Crowl A.A., Mavrodiev E., Cellinese N., Oanesian M., Fraunhofer K., Kamari G., Phitos D., Haberle R., Akaydin G., Ikinci N., Raus T. & Borsch T. 2012: How to Handle Speciose Clades? Mass Taxon-Sampling as a Strategy towards Illuminating the Natural History of Campanula (Campanuloideae). – PLoS ONE7 (11) .
McVaugh R. 1945: The genus Triodanis Rafinesque, and its relationships to Specularia and Campanula. – Wrightia 1: 13–52.
Rechinger K. & Schiman-Czeika H. 1965: Campanulaceae – Pp. 141–159 in: Rechinger K., (ed.). Flora Iranica. – Graz: Akademische Druck- und Verlagsanstalt.
Roquet C., Saez L., Aldasoro J.J., Susanna A., Alarcon M.L. & al. 2008: Natural delineation, molecular phylogeny and floral evolution in Campanula. – Syst. Bot.33: 203–217 .
Shetler S.G. & Morin N.R. 1986: Seed morphology in North American Campanulaceae. – Ann. Missouri Bot. Gard.73: 653–688 .
Weigend M., Gottschling M., Selvi F. & Hilger H.H. 2009: Marbleseeds are gromwells – Systematics and evolution of Lithospermum and allies (Boraginaceae tribe Lithospermeae) based on molecular and morphological data. – Mol. Phylogenet. Evol.52: 775–768 .
Wendling B.M., Galbreath K.E. & DeChaine E.G. 2011: Resolving the evolutionary history of Campanula (Campanulaceae) in Western North America. – PLoS ONE 6 (9) .
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)
References
Allan G.J. & Porter J.M. 2000: Tribal delimitation and phylogenetic relationships of Lotea and Coronilleae (Faboideae: Fabaceae) with special reference to Lotus: evidence from nuclear ribosomal ITS sequences. – Amer. J. Bot.
Cellinese N., Smith S.A., Edwards E..J, Kim S.T., Haberle R.C., & al. 2009: Historical biogeography of the endemic Campanulaceae of Crete. – J. Biogeogr.
Damboldt J. 1978: Campanulaceae – Pp. 2–65 in: Davis PH., (ed.), Flora of Turkey and the East Aegean Islands. – Edinburgh: University Press.
Drummond C.S. 2008: Diversification of Lupinus (Leguminosae) in the western New World: Derived evolution of perennial life history and colonization of montane habitats. – Mol. Phylogenet. Evol.
Eddie W.M.M. & Ingrouille M.J. 1999: Polymorphism in the Aegean “five-loculed” species of the genus Campanula, Section Quinqueloculares (Campanulaceae). – Nord. J. Bot.
Frajman B. & Schneeweiss G.M. 2009: A Campanulaceous Fate: The Albanian Stenoendemic Asyneuma comosiforme in Fact Belongs to Isophyllous Campanula. – Syst. Bot.
Haberle R.C., Dang A., Lee T., Penaflor C., Cortes-Burns H., & al. 2009: Taxonomic and biogeographic implications of a phylogenetic analysis of the Campanulaceae based on three chloroplast genes. – Taxon
Hohmann S., Kadereit J.W. & Kadereit G. 2006: Understanding Mediterranean-Californian disjunctions: Molecular evidence from Chenopodiaceae-Betoideae. – Taxon
Lammers T.G. 2007: World checklist and bibliography of Campanulaceae. – Kew: Royal Botanical Garden. 675 p.
Mansion G. & Struwe L. 2004: Generic delimitation and phylogenetic relationships within the subtribe Chironiinae (Chironieae : Gentianaceae), with special reference to Centaurium: evidence from nrDNA and cpDNA sequences. – Mol. Phylogenet. Evol.
Mansion G. & Zeltner L. 2004: Phylogenetic relationships within the new world endemic Zeltnera (Gentianaceae-Chironiinae) inferred from molecular and karyological data. – Amer. J. Bot.
Mansion G., Parolly G., Crowl A.A., Mavrodiev E., Cellinese N., Oanesian M., Fraunhofer K., Kamari G., Phitos D., Haberle R., Akaydin G., Ikinci N., Raus T. & Borsch T. 2012: How to Handle Speciose Clades? Mass Taxon-Sampling as a Strategy towards Illuminating the Natural History of Campanula (Campanuloideae). – PLoS ONE
McVaugh R. 1945: The genus Triodanis Rafinesque, and its relationships to Specularia and Campanula. – Wrightia 1: 13–52.
Rechinger K. & Schiman-Czeika H. 1965: Campanulaceae – Pp. 141–159 in: Rechinger K., (ed.). Flora Iranica. – Graz: Akademische Druck- und Verlagsanstalt.
Roquet C., Saez L., Aldasoro J.J., Susanna A., Alarcon M.L. & al. 2008: Natural delineation, molecular phylogeny and floral evolution in Campanula. – Syst. Bot.
Shetler S.G. & Morin N.R. 1986: Seed morphology in North American Campanulaceae. – Ann. Missouri Bot. Gard.
Weigend M., Gottschling M., Selvi F. & Hilger H.H. 2009: Marbleseeds are gromwells – Systematics and evolution of Lithospermum and allies (Boraginaceae tribe Lithospermeae) based on molecular and morphological data. – Mol. Phylogenet. Evol.
Wendling B.M., Galbreath K.E. & DeChaine E.G. 2011: Resolving the evolutionary history of Campanula (Campanulaceae) in Western North America. – PLoS ONE