Phylogenetics and evolution of Euphorbia subgenus Chamaesyce.

Abstract

Euphorbia subg. Chamaesyce Raf. contains about 600 species and includes the largest New World radiation within the Old World-centered Euphorbia (Euphorbiaceae). It is one of the few plant lineages to include members with C3, C4 and CAM photosynthesis, showing multiple adaptations to warm and dry habitats. The subgenus includes North American-centered groups that were previously treated at various taxonomic ranks under the names of “Agaloma”, “Poinsettia,” and “Chamaesyce”. Here we provide a well-resolved phylogeny of Euphorbia subg. Chamaesyce using nuclear ribosomal ITS and chloroplast ndhF sequences, with substantially increased taxon sampling compared to previous studies. Based on the molecular phylogeny, we discuss the Old World origin of the subgenus, the evolution of cyathial morphology and growth forms, and then we provide a formal subgeneric classification, with descriptions and species lists for each section or subsection we recognize. Among the fifteen sections we recognized within subg. Chamaesyce, sect. Anisophyllum is the largest lineage of C4 plants among the eudicots, with 350 species including both narrow endemics and cosmopolitan weeds. We sampled this group worldwide with 138 ingroup species, using two nuclear (ITS and exon 9 of EMB2765) and three chloroplast markers (matK, rpl16, and trnL-F). Three major clades were recovered within the section [1(2,3)]: (1) the Acuta clade, containing three North American species with C3 photosynthesis and C3-C4 intermediates; (2) the Peplis clade, mostly North American and entirely C4; and (3) the Hypericifolia clade, all C4, with both New World and Old World groups. Incongruence between chloroplast and ITS phylogenies and divergent cloned copies of EMB2765 exon 9 suggest extensive hybridization. Woody members of sect. Anisophyllum originated once from herbaceous members in the New World, probably through allopolyploidy, and diversified into 16 species that occupy all habitat types on the major Hawaiian islands. We further increased taxon sampling within the Hawaiian radiation to 104 ingroup accessions including 15 of the 16 species. Chloroplast data including more than 8 kb of non-coding regions support old to young island dispersal along the Hawaiian island chain. Nuclear ITS, LEAFY and G3pdhC markers further support the hybrid origin of Hawaiian Anisophyllum with recent interspecific hybridizations.