Evolutionary diversification of the African Achyranthoid clade (Amaranthaceae) in the context of sterile flower evolution and epizoochory. African Achyranthoids

BACKGROUND AND AIMS: Many African genera of the Amaranthaceae exhibit unique inflorescences that include sterile flowers modified to hooks or spines. Considering that the abundance of large terrestrial herbivores increased on the African continent with the expansion of grassland and savannah ecosystems, modified sterile flowers could have been an innovation that boosted the diversification of an African Achyranthoid clade of Amaranthaceae, with large animals serving dispersal. METHODS: We generated an extensively-sampled phylogeny comprising 26 of the 31 Achyranthoid genera as well as representatives of all other lineages of Amaranthaceae. Phylogenetic tree inference employed four genomic regions, using parsimony, likelihood and Bayesian inference methods. We estimated divergence times, evaluated trait-dependant changes and species diversification rates using state-dependent speciation and extinction models, and reconstructed ancestral character states for modified sterile flowers. KEY RESULTS: The Achyranthoids were found a major clade of the Amaranthaceae, comprising mostly African members. Phylogenetic relationships within this clade were well-resolved and supported two main subclades. Several genera were found polyphyletic. Our results indicate that the Achyranthoids started to diversify c. 28 Ma ago, and that modified sterile flowers evolved multiple times. An asymmetry in transition rates towards the gain of sterile flowers is observed, whereas no trait-dependant increase of species diversification rates was detected. Bayesian rate heterogeneity analyses indicated that the Achyranthoids diversified without significant rate shifts. CONCLUSIONS: The accumulation of modified sterile flowers within Achyranthoids appears to result from the higher transition rates in favour of modified sterile flowers. Multiple gains suggest an adaptive value for this trait. However, epizoochory does not appear to fuel species diversification, possibly due to extensive gene flow through regularly migrating mammals which limits the possibility for speciation by isolation.