Phylogeny, biogeography and ecological diversification of Sarcocornia (Salicornioideae, Amaranthaceae)

Background and Aims Sarcocornia comprises about 28 species of perennial succulent halophytes distributed worldwide, mainly in saline environments of warm-temperate and subtropical regions. The genus is characterized by strongly reduced leaves and flowers, which cause taxonomic difficulties; however, species in the genus show high diversity in growth form, with a mat-forming habit found in coastal salt marshes of all continents. Sarcocornia forms a monophyletic lineage with Salicornia whose species are all annual, yet the relationship between the two genera is poorly understood. This study is aimed at clarifying the phylogenetic relationship between Sarcocornia and Salicornia, interpreting biogeographical and ecological patterns in Sarcocornia, and gaining insights into putative parallel evolution of habit as an adaptation to environmental factors. Methods A comprehensively sampled and dated phylogeny of Sarcocornia is presented based on nuclear ribosomal DNA (external transcribed spacer) and chloroplast DNA (atpB-rbcL, rpl32-trnL) sequences; representative samples of Salicornia were also included in the analyses. To infer biogeographical patterns, an ancestral area reconstruction was conducted. Key Results The Sarcocornia/Salicornia lineage arose during the Mid-Miocene from Eurasian ancestors and diversified into four subclades: the Salicornia clade, the American Sarcocornia clade, the Eurasian Sarcocornia clade and the South African/Australian Sarcocornia clade. Sarcocornia is supported as paraphyletic, with Salicornia nested within Sarcocornia being sister to the American/Eurasian Sarcocornia clade. The American and the South African/Australian Sarcocornia clade as well as the Salicornia clade were reconstructed to be of Eurasian origin. The prostrate, mat-forming habit arose multiple times in Sarcocornia. Conclusions Sarcocornia diversified in salt-laden environments worldwide, repeatedly evolving superficially similar prostrate, mat-forming habits that seem advantageous in stressed environments with prolonged flooding, high tidal movement and frost. Some of these prostrate-habit types might be considered as ecotypes (e.g. S. pacifica or S. pillansii) while others represent good ecospecies (e.g. S. perennis, S. decumbens, S. capensis), hence representing different stages of speciation.