Allopolyploidy, diversification, and the Miocene grassland expansion

Abstract

The role of polyploidy, particularly allopolyploidy, in plant diversification is a subject of debate. Whole-genome duplications precede the origins of many major clades (e.g., angiosperms, Brassicaceae, Poaceae), suggesting that polyploidy drives diversification. However, theoretical arguments and empirical studies suggest that polyploid lineages may actually have lower speciation rates and higher extinction rates than diploid lineages. We focus here on the grass tribe Andropogoneae, an economically and ecologically important group of C4 species with a high frequency of polyploids. A phylogeny was constructed for ca. 10% of the species of the clade, based on sequences of four concatenated low-copy nuclear loci. Genetic allopolyploidy was documented using the characteristic pattern of double-labeled gene trees. At least 32% of the species sampled are the result of genetic allopolyploidy and result from 28 distinct tetraploidy events plus an additional six hexaploidy events. This number is a minimum, and the actual frequency could be considerably higher. The parental genomes of most Andropogoneae polyploids diverged in the Late Miocene coincident with the expansion of the major C4 grasslands that dominate the earth today. The well-documented whole-genome duplication in Zea mays ssp. mays occurred after the divergence of Zea and Sorghum. We find no evidence that polyploidization is followed by an increase in net diversification rate; nonetheless, allopolyploidy itself is a major mode of speciation.

Fig. 1.

Chronogram of the phylogeny of Andropogoneae produced in BEAST (57). Branch colors indicate Bayesian posterior probability with red highest, green lowest. Numbers, allotetraploidization events; letters, allohexaploidization events; black dots, common ancestors of the parental genomes of the polyploids; gray dots, accessions with large, likely polyploid, genome sizes but without evidence of genetic allopolyploidy; shading, approximate time of the Miocene grassland expansion. The order in which the hexaploid genomes came together is unknown; for clarity, they are drawn as though a tetraploid formed from the most closely related parents, and the hexaploidy event added the more distant one, but this is merely a graphical convention.

Fig. 2.

(A) Phylogeny of the Bothriochloa-Capillipedium-Dichanthium clade, showing the complex history of B. bladhii, which combines genomes of all three genera in plants that are morphologically placed in Bothriochloa. Numbered polyploidization events correspond to those in Fig. 1 and Figs. S2 and S3. For species with more than one accession, accession numbers follow the species name. Black lines connect genomes of tetraploids, and gray lines connect hexaploids. (B) Summary of data from extensive crossing experiments and chromosome pairing studies [redrawn from de Wet and Harlan (42)]. The genomic history inferred from cytogenetics is congruent with that in our phylogenetic study. Green shading, Dichanthium genomes; yellow shading, Capillipedium genomes; dark green and dark yellow shading, Bothriochloa accessions bearing Dichanthium and Capillipedium genomes, respectively.