Gomphrena (Amaranthaceae, Gomphrenoideae) diversified as a C4 lineage in the New World tropics with specializations in floral and inflorescence morphology, and an escape to Australia

Abstract

The genus Gomphrena comprises about 120 species in the Americas and 35 in Australia. Previous research revealed that Gossypianthus, Lithophila and Philoxerus are closely related but the monophyly of Gomphrena remained unresolved. Our aim was to clarify phylogenetic relationships in Gomphrena and allies based on a thorough sampling of species and to reconstruct the evolution of morphological characters including C-4 photosynthesis, and to explore the disjunction of the Australian taxa. We generated datasets of plastid (matK-trnK, trnL-F, rpl16) and nrITS representing 45 taxa of Gomphrena plus relatives and analysed them with parsimony, likelihood and Bayesian methods. Ancestral states of phenotypic characters were reconstructed with BayesTraits. BEAST was employed for divergence time estimates using an extended Amaranthaceae-Chenopodiaceae dataset to place fossil calibration points. Gossypianthus is closely related to a Gomphrena radiata-G. umbellata G. tomentosa Blade and G. meyeniana, whereas Lithophila and Philoxerus appear as successive sisters of the Australian species of Gomphrena. The majority of Andean species appears in a large Glade including annual and perennial species. The Cerrado species Gomphrena mollis and G. rupestris, which are C-3, constitute an early-branching lineage, whereas the core Gomphrena Glade is C-4 and has the inner two sepals strongly compressed as synapomorphy. A major subclade evolved inflorescences with subglobose paracladia in a whorl, supported by pseudanthial leaves. Whereas the core Gomphrena Glade started to diversify around 11.4 Ma (8.45-14.5 95% highest posterior density [HPD]) the Australian lineage split at only 4.8 Ma (2.61- 7.18 HPD). Our detailed phylogenetic analysis of Gomphrena depicts 10 major lineages including segregate genera. We hypothesize that an adaptation to costal habitats was followed by long-distance dispersal to Australia. We also propose a revised genus concept of Gomphrena including Gossypianthus, Lithophila and Philoxerus, considering that these small segregate genera were based on states of vegetative characters exhibiting adaptations to specific habitats rather than phylogeny and overall morphology.