Phylogenetics, evolution and biogeography of four Digitaria food crop lineages across West Africa, India, and Europe

Abstract Background and Aims Millet crops in the grass genus Digitaria include white and black fonio ( D. exilis and D. iburua ), raishan ( D. compacta ) and Polish millet ( D. sanguinalis ), cultivated across West Africa, India, and Europe. Fonio and raishan crops are important to supporting food security and subsistence agricultural systems in rural communities, while D. sanguinalis is no longer cultivated. These crops are resilient to challenging climates. We aim to produce an integrated study of these crops: a phylogeny of the Digitaria genus including all four food species, to identify key crop wild relatives (CWRs); time-calibrated biogeographic analysis, to investigate the history and evolution of Digitaria ; and morphological study to assess the transition between wild and domesticated species. Methods We use the Angiosperm 353 target-enrichment sequencing approach to produce maximum likelihood and coalescent model nuclear phylogenies for 46 Digitaria species, including ploidy estimations, and bayesian methods to propose an evolutionary and biogeographic history for the genus. Morphology of wild and cultivated species is investigated for spikelets and growth habits using microscopy and SEM imaging techniques. Key Results Four distinct lineages are proposed for the evolution of Digitaria crops, and close CWRs D. fuscescens , D. atrofusca , D. setigera and D. radicosa , and D. ciliaris are identified. South and eastern Africa is proposed as the origin of early Digitaria divergence, with crop lineages diverging from wild relatives around 2-6mya. Incomplete domestication traits are observed, including the loss of trichomes, but no significant difference in spikelet or abscission zone morphology. Conclusions Digitaria crops have important climate-resilient traits and hold strong potential for stabilising vulnerable food systems against the challenges of future climate change. The knowledge produced in this study about CWRs will be useful in improving crop traits through targeted breeding and indigenous crop conservation programmes.