Molecular phylogeny of Camphorosmeae (Camphorosmoideae, Chenopodiaceae): Implications for biogeography, evolution of C4-photosynthesis and taxonomy

Camphorosmeae constitute a species-rich tribe of Chenopodiaceae-Camphorosmoideae that consists mostly of subshrubs and annuals, distributed in steppes and semi-deserts of Australia, Eurasia, North Africa, southern Africa and North America. We study (1) the relationships of Camphorosmeae to major lineages of the closely related Salsoloideae and (2) the diversification of the tribe with focus on the non-Australian members using sequence variation of five different markers (rbcL gene, ndhF gene, atpB-rbcL spacer, psbB-psbH spacer, ITS) and morphological characters. The cpDNA analyses revealed six early-branching lineages in Camphorosmoideae/Salsoloideae (Camphorosmeae, Salsoleae s.str., Caroxyloneae, Salsola kali clade, Nanophyton clade, Salsola genistoides clade) and supported partly (ndhF and atpB-rbcL spacer) the sister-group relationship of Camphorosmeae and all Salsolean clades. The distinctness of Camphorosmeae and Salsoleae s.l. is further supported by seed, stigma and pollen morphology. Molecular clock estimates point to an earlier radiation in Salsoleae s.l. (Early to Middle Oligocene) than in Camphorosmeae (Early Miocene). In Salsoleae s.l. early radiation might have been enhanced by multiple evolution of C4-photosynthesis which facilitated the spread into drier habitats of Eurasia. In Camphorosmeae, C4-photosynthesis likely evolved two times, probably in the Middle Miocene. During the Miocene Camphorosmeae spread from Eurasia to Australia, North America and at least two times to South Africa. Only the Australian lineage diversified, the others remained species-poor. The molecular trees congruently resolve three major clades of unclear relationship within Camphorosmeae, Chenolea clade (five widely disjunct and morphologically divergent C3-species, possibly remnants of old lineages), Sclerolaena clade (ca. 150 C3-species from Central Asia [3 spp.] and Australia [147 spp.], probably the results of a rapid radiation during the Pliocene) and Bassia/Camphorosma clade (ca. 23 C4-species and one C3/C4-intermediate which are widely distributed in Eurasia and southern Africa). The phylogenies show the artificial state of the current generic and subtribal classifications of Eurasian, North American and South African Camphorosmeae. All non-monotypic genera except Camphorosma and Neokochia were found to be polyphyletic. A revised classification of the tribe is proposed including reinstatement of the newly defined subfamily Camphorosmoideae, description of the new genera Spirobassia (1 sp.), Eokochia (1 sp.), Grubovia (3 spp.) and Sedobassia (1 sp.), and several new combinations and synonymizations.