Deep homology and developmental constraint underlie the replicated evolution of grass awns

Replicated trait evolution can provide insights into the mechanisms underlying the evolution of biodiversity. One example of replicated evolution is the awn, an organ elaboration in grass inflorescences. Awns are likely homologous to leaf blades. We hypothesized that awns have evolved repeatedly because a conserved leaf blade developmental program is continuously activated and suppressed over the course of evolution, leading to the repeated emergence and loss of awns. To evaluate predictions arising from our hypothesis, we used ancestral state estimations, comparative genetics, anatomy, and morphology to trace awn evolution. In line with our predictions, we discovered that awned lemmas that evolved independently share similarities in anatomy and developmental trajectory. In addition, in two species with independently derived awns and differing awn morphologies (Brachypodium distachyon and Alopecurus myosuroides), we found that orthologs of the YABBY transcription factor gene DROOPING LEAF are required for awn initiation. Our analyses of awn development in Brachypodium distachyon, Alopecurus myosuroides, and Holcus lanatus also revealed that differences in the relative expansion of awned lemma compartments can explain diversity in awn morphology at maturity. Our results show that developmental conservation can underlie replicated evolution, and can potentiate the evolution of morphological diversity.