Developmental constraint underlies the replicated evolution of grass awns

New Phytol. 2024 Nov 18. doi: 10.1111/nph.20268. Online ahead of print.

Abstract

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. We discovered that awned lemmas that evolved independently share similarities in 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.

Keywords: ancestral developmental potential; convergent evolution; developmental constraint; flower development; grass evolution; leaf development; parallel evolution; plant evo‐devo.