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Evolutionary dynamics of serpentine adaptation in Onosma (Boraginaceae) as revealed by ITS sequence data

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Abstract

Plant life on serpentine soils has been a topic of research for decades, but the evolutionary dynamics of adaptation to such a stressful habitat is still incompletely understood, especially in old-world groups. We present a study addressing this issue using Onosma (Boraginaceae) as the model system and a molecular phylogenetic approach. Original ITS sequences were generated for all the obligate endemics allopatrically distributed on the ophiolitic “islands” of the southeastern Euro-Mediterranean region, in addition to most of the species facultatively growing on ultramafics and a broad sample of non-serpentine species. Parsimony and Bayesian reconstructions showed that obligate endemics belonged to six distantly related clades, five continental and one insular in the Aegean sea (Cyprus). Lack of a common ancestor and of correlation between geographic and genetic distances between the endemics suggested polyphyletic and polytopic evolution on the different outcrops. Preference for non-serpentine habitats appeared as the ancestral condition, but constitutive preadaptive traits such as drought tolerance and ability to cope with high soil concentrations of magnesium have probably favoured multiple events in the colonization of ultramafics. Tree topology and absolute age estimations suggest that xerophytic Onosma underwent a rapid radiation in correspondence with the Messinian salinity crisis of the Mediterranean (6–5.3 mya), and that the endemic lineages originated at the beginning of the Pleistocene. Serpentine “islands” may have acted as refugial habitats during the cold climatic phases, and then as major determinants of adaptive speciation due to isolation of populations and the selective pressure of soil constraints.

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Acknowledgments

The authors wish to thank H.H. Hilger, M. Weigend (Berlin) and F. Pushtajia (Sarajevo), for providing material of Onosma; L. Pignotti (Wien) and the curators of the herbaria cited in “Materials and methods” for allowing study of their collections. Two anonymous reviewers provided useful comments on the first version of the manuscript. Research grants from the University of Firenze and the Italian Ministry for Scientific Research are acknowledged.

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  1. Department of Evolutionary Biology, Botanical Laboratories, Via G. La Pira 4, 50121, Florence, Italy

    L. Cecchi

  2. Department of Agricultural Biotechnology, Section of Applied and Environmental Botany, 50144, Florence, Italy

    A. Coppi & F. Selvi

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  1. L. Cecchi
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Correspondence to L. Cecchi.

Appendix

Appendix

List of GenBank accessions of additional species analyzed to define the time-frame for the evolution of Onosma (see Fig. 3):

Cerinthe glabra, FJ541016; Echium acanthocarpum, EU048853.1; E. aculeatum, EU048849.1; L43169; E. albicans, L43172; E. arenarium, EU919584; E. asperrimum, L43176; E. auberianum, L43180; E. bonnetii, L43184; E. brevirame, L43188; E. callithyrsum, L43196; E. candicans, EU048856.1; L43192; E. creticum, FJ763249; L43208; E. decaisnei, EU048852.1; L43212; E. giganteum, L43224; E. handiense, L43220; E. hierrense, EU048848.1; L43216; E. horridum, L43228; E. humile, AF284109; E. hypertropicum, EU048858.1; L43232; E. italicum, L43236; E. leucophaeum, L43240; E. lusitanicum, EU048847.1; L43252; E. nervosum, EU048855.1; L43256; E. onosmaefolium, L43260; E. parviflorum, L43264; E. pininana, L43268; E. pitardii, L43322; E. plantagineum, L43272; E. pycnanthum, AF284108; E. rosulatum, L43276; E. sabulicola, L43288; E. simplex, EU048851.1; L43284; E. stenosiphon, EU048859.1; L43319; E. strictum, L43292; E. tenue subsp. dumosum, AF284106; E. triste, L43324; E. tuberculatum, L43300; E. vilmorinianum, AF284107; E. virescens, EU048850.1; L43296; E. vulcanorum, EU048857.1; L43304; E. vulgare, AJ555896; AY092900; FJ763247; FJ789862; L43312; E. webbii, EU048854.1; L43308; E. wildpretii, L43316; Moltkia petraea, EU919596.

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Cecchi, L., Coppi, A. & Selvi, F. Evolutionary dynamics of serpentine adaptation in Onosma (Boraginaceae) as revealed by ITS sequence data. Plant Syst Evol 297, 185–199 (2011). https://doi.org/10.1007/s00606-011-0506-3

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