Phylogeny of Salicornioideae (Chenopodiaceae): diversification, biogeography, and evolutionary trends in leaf and flower morphology

Chenopodiaceae-Salicornioideae (14-16 gen./c. 90 spp.) are distributed worldwide in coastal and inland saline habitats. Most of them are easy to recognize by their succulent-articulated stem with strongly reduced leaves and by flowers aggregated in dense, thick spike-shaped thyrses. ITS and the atpB-rbcL spacer were sequenced for 67 species representing 14 genera of Salicornioideae and analysed with maximum parsimony and maximum likelihood, a fossil-calibrated molecular clock using the penalized likelihood method, and lineage through time plots. The evolution of stem, leaf, and flower morphology was traced using MacClade. Both molecular markers indicate that the monophyletic Salicornioideae originated in Eurasia during the Late Eocene/Early Oligocene (38.2-28.7 Mya) and experienced a rapid radiation into its major lineages during the Early Oligocene with Allenrofea/Heterostachys, Kalidium, Halopeplis and Halocnemum/Halostachys branching off early. Already in the Middle Miocene (19.6-14.6 Mya) all major lineages of Salicornioideae were present. These additionally include Arthrocnemum/Microcnemum, the Halosarcia lineage (which includes all Australian species except for the Australian Sarcocornia) and the Salicornia/Sarcocornia lineage. A high intercontinental dispersability can be observed in Salicornioideae in particular in the Salicornia/Sarcocornia lineage with multiple colonization events in America, Australia and South Africa linked to the global aridification during the Oligocene, Late Miocene and Pliocene. The comparatively low species number of many genera is explained by a low number of niches present in the extreme habitats of Salicornioideae, strong interspecific competition mainly by close relatives, and by Pleistocene extinctions. We detected an evolutionary trend towards increasing reduction of the leaf lamina in Salicornioideae, with an ovate or terete leaf with a decurrent base as the plesiomorphic condition. Opposite phyllotaxis has arisen at least two times in the subfamily and is strongly correlated with the pair-wise fusion of leaves (not bracts), the reduction of leaf lamina, and the articulation of stem. However, the articulated stems and reduced leaves also have evolved twice in lineages with alternate phyllotaxis, such as Allenrofea and Kalidium caspicum. Only one shift from free to connate bracts occurred in Salicornioideae with at least one reversal within the Halosarcia lineage. The fusion of bracts is mostly accompanied by a partly or fully connation of bracts and axis resulting in club-shaped spikes in which the flowers are tightly embedded in cavities. Both molecular trees are conflicting with the traditional tribes indicating that their diagnostic characters have originated by convergent evolution. For reasons of stability and clarity we propose that only one tribe, Salicornieae, should be recognized. The traditional circumscription of 9 most genera is supported by the molecular results except for the closely related genera of the Australian Halosarcia clade and the Sarcocornia/Salicornia complex. The monotypic Kalidiopsis clearly originated from within Kalidium, and it is therefore newly combined in Kalidium.