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 C 4 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 C 4 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. P olyploidy (whole-genome duplication) is often linked with the acquisition of new traits and subsequent species diversification, particularly in plants (1, 2). Ancient polyploidy correlates with major land-plant radiations (3) and the origins of orders, large families, and major clades (4-7) although, in many cases, sharp changes in diversification rates are delayed for millions of years after the polyploidization event (1). This phylogenetic pattern has led to the hypothesis that polyploidy causes or promotes diversification. Good mechanistic reasons support such a hypothesis. Studies of naturally occurring and synthetic polyploids find changes in gene expression, gene loss, release of transposons, and changes in morphology and physiology immediately after polyploidy (4,(8)(9)(10)(11)(12)). This pattern is particularly true for allopolyploids, which originate from a cross between genetically distinct parents often representing different species; in such cases, the biological changes seen after polyploidization may not reflect the effects of genome doubling per se, but rather the effect of hybridization between distantly related progenitors (4).Despite the appeal of the hypothesis that polyploidy causes diversification, there is evidence to the contrary. As noted by Stebbins (13), "polyploidy has been important in the diversification of species and genera within families, but not in the origin of the families and orders themselves," implying that polyploidy is only a minor force in diversification (see also ref. 14). ...

Phylogenomics of Andropogoneae (Panicoideae: Poaceae) of Mainland Southeast Asia

“…Estep et al 2014), probably as a result of our sample of more disparate members of the genus. Although this study still includes only a fraction of the species in the genus, we think it is unlikely that inclusion of additional species will cause Andropogon to appear as monophyletic.…”

“…One group of S. sanguineum plastomes clustered with American Schizachyrium (S. scoparium and S. spicatum) and the other with Asian species (S. exile and S. brevifolium). All S. sanguineum samples were collected in Thailand, suggesting either a deep coalescence of chloroplast haplotypes within S. sanguineum that predate the geographical disjunction of other Schizachyrium species or admixture of haplotypes through allopolyploidy as discussed below (Peichoto et al 2011;Estep et al 2014).…”

“…The phylogeny of the tribe has been difficult to resolve, apparently because of a rapid radiation early in the evolution of the tribe (Mathews et al 2002;Spangler et al 1999;Bouchenak-Khelladi et al 2008). However, by using multiple concatenated nuclear genes, Estep et al (2014) were able to identify early-diverging lineages including Arthraxon, Chrysopogon Trin., and a Zea-Tripsacum clade, a somewhat miscellaneous grade of smaller groups, and a Saccharum L. clade. About half of the species in the tribe were placed in a large well-supported clade that they called informally "the core Andropogoneae."…”

“…Considering the Andropogoneae as a whole, two of the largest genera of the core are Andropogon and Schizachyrium, which together form a clade (Giussani et al 2001;Mathews et al 2002;Skendzic et al 2007;Teerawatananon et al 2011;Estep et al 2014). These are major grasses for forage and ecosystems and have been used as representatives for many studies in ecology, taxonomy, and phylogenetics.…”

“…Mimulus L.; Vallejo-Marín et al 2016). The versatility of whole chloroplast genomes to resolve intrageneric relationships is promising for establishing evolutionary relationships in Andropogoneae of mainland Southeast Asia, an intratribal taxonomic issue spanning 26 million years (Estep et al 2014).…”