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Physiological diversity enhanced by recurrent divergence and secondary gene flow within a grass species

Matheus E. Bianconi,L. Dunning,E. Curran,O. Hidalgo,R. Powell,Sahr Mian,I. Leitch,M. Lundgren,S. Manzi,M. Vorontsova,G. Besnard,C. Osborne,Jill K. Olofsson,P. Christin

Published 2020 in bioRxiv

ABSTRACT

C4 photosynthesis evolved multiple times independently in angiosperms, but most origins are relatively old so that the early events linked to photosynthetic diversification are blurred. The grass Alloteropsis semialata is an exception, as this single species encompasses C4 and non-C4 populations. Using phylogenomics and population genomics, we infer the history of dispersal and secondary exchanges before, during, and after photosynthetic divergence in A. semialata. We further establish the genetic origins of polyploids in this species. Organelle phylogenies indicate limited seed dispersal within the Central Zambezian region of Africa, where the species originated ∼ 2–3 Ma. Outside this region, the species spread rapidly across the paleotropics to Australia. Comparison of nuclear and organelle phylogenies and analyses of whole genomes reveal extensive secondary gene flow. In particular, the genomic group corresponding to the C4 trait was swept into seeds from distinct geographic regions. Multiple segmental allopolyploidy events mediated additional secondary genetic exchanges between photosynthetic types. Limited dispersal and isolation allowed lineage divergence, while episodic secondary exchanges led to the pollen-mediated, rapid spread of the derived C4 physiology. Overall, our study suggests that local adaptation followed by recurrent secondary gene flow promoted physiological diversification in this grass species.

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