Phylogenomics and Systematics of Overlooked Mesoamerican and South American Polyploid Broad-Leaved Festuca Grasses Differentiate F. sects. Glabricarpae and Ruprechtia and F. subgen. Asperifolia, Erosiflorae, Mallopetalon and Coironhuecu (subgen. nov.)

Abstract

Allopolyploidy is considered a driver of diversity in subtribe Loliinae. We investigate the evolution and systematics of the poorly studied Mesoamerican and South American polyploid broad-leaved Festuca L. species of uncertain origin and unclear taxonomy. A taxonomic study of seven diagnostic morphological traits was conducted on a representation of 22 species. Phylogenomic analyses were performed on a representation of these supraspecific taxa and all other Loliinae lineages using separate data from the entire plastome, nuclear rDNA 45S and 5S genes, and repetitive DNA elements. F. subgen. Mallopetalon falls within the fine-leaved (FL) Loliinae clade, whereas the remaining taxa are nested within the broad-leaved (BL) Loliinae clade forming two separate Mexico-Central-South American (MCSAI, MCSAII) lineages. MCSAI includes representatives of F. sect. Glabricarpae and F. subgen. Asperifolia plus F. superba, and MCSAII of F. subgen. Erosiflorae and F. sect. Ruprechtia plus F. argentina. MCSAII likely had a BL Leucopoa paternal ancestor, MCSAI and MCSAII a BL Meso-South American maternal ancestor, and Mallopetalon FL, American I-II ancestors. Plastome vs. nuclear topological discordances corroborated the hybrid allopolyploid origins of these taxa, some of which probably originated from Northern Hemisphere ancestors. The observed data indicate rapid reticulate radiations in the Central-South American subcontinent. Our systematic study supports the reclassification of some studied taxa in different supraspecific Festuca ranks.

Keywords: Mexico–Central–South American broad-leaved Festuca; allopolyploid speciation; phylogeny; plastome; rDNA 45S and 5S genes; repeatome; taxonomy.

Figure 1

Ligule shape of representative species of Mesoamerican and South American broad-leaved Festuca taxa analyzed morphologically in this study. F. subgen. Subulatae sect. Glabricarpae: F. venezuelana (a); F. subgen. Drymanthele s. l.: F. superba (b); F. subgen. Subulatae sect. Glabricarpae: F. breviglumis (c); F. subgen. Asperifolia: F. asperella (d); F. subgen. Erosiflorae: F. quadridentata (e,f); F. subgen. Drymanthele sect. Ruprechtia: F. amplissima (g); F. subgen. Coironhuecu (subgen. nov.): F. argentina (h); F. subgen. Mallopetalon: F. fimbriata (i). Drawings by José Alfredo Hidalgo-Salazar (a–h) and María Fernanda Moreno-Aguilar (i). ((a,f): modified from Stančík and Peterson [31]; (b): modified from Türpe [49]; (c): Peterson P. M. and Rosales O. 16117, US-3524155; (d): Dziekanowski et al., 2022, MO-2107299 (isotype); (e): Laegaard S. 55567, AAU; (g): Peterson P. M. and Herrera-Arrieda Y. 16150, US-3524157; (h): modified from Ospina [34]; (i): Kostling M. UZ 498.08).

Figure 2

Maximum likelihood phylogenomic trees of the Mesoamerican and South American broad-leaved Festuca taxa studied and other representative species of the broad-leaved (BL) and fine-leaved (FL) Loliinae lineages. (a) Nuclear rDNA 35S cistron tree. (b) Nuclear rDNA (45S) IGS tree. (c) Nuclear rDNA 5S tree. (d) Plastome tree. Mexico–Central–South American (MCSAI, MCSAII) and Mallopetalon groups are indicated by discontinuous-line rectangles. Ultrafast bootstrap support values are indicated on branches. Oryza sativa and Brachypodium distachyon outgroups were used to root the trees except for the IGS and 5S trees that were rooted at midpoint. Color codes of Loliinae lineages are indicated in the chart of (a). Scale bars: number of mutations per site.

Figure 2

Maximum likelihood phylogenomic trees of the Mesoamerican and South American broad-leaved Festuca taxa studied and other representative species of the broad-leaved (BL) and fine-leaved (FL) Loliinae lineages. (a) Nuclear rDNA 35S cistron tree. (b) Nuclear rDNA (45S) IGS tree. (c) Nuclear rDNA 5S tree. (d) Plastome tree. Mexico–Central–South American (MCSAI, MCSAII) and Mallopetalon groups are indicated by discontinuous-line rectangles. Ultrafast bootstrap support values are indicated on branches. Oryza sativa and Brachypodium distachyon outgroups were used to root the trees except for the IGS and 5S trees that were rooted at midpoint. Color codes of Loliinae lineages are indicated in the chart of (a). Scale bars: number of mutations per site.

Figure 2

Maximum likelihood phylogenomic trees of the Mesoamerican and South American broad-leaved Festuca taxa studied and other representative species of the broad-leaved (BL) and fine-leaved (FL) Loliinae lineages. (a) Nuclear rDNA 35S cistron tree. (b) Nuclear rDNA (45S) IGS tree. (c) Nuclear rDNA 5S tree. (d) Plastome tree. Mexico–Central–South American (MCSAI, MCSAII) and Mallopetalon groups are indicated by discontinuous-line rectangles. Ultrafast bootstrap support values are indicated on branches. Oryza sativa and Brachypodium distachyon outgroups were used to root the trees except for the IGS and 5S trees that were rooted at midpoint. Color codes of Loliinae lineages are indicated in the chart of (a). Scale bars: number of mutations per site.

Figure 2

Maximum likelihood phylogenomic trees of the Mesoamerican and South American broad-leaved Festuca taxa studied and other representative species of the broad-leaved (BL) and fine-leaved (FL) Loliinae lineages. (a) Nuclear rDNA 35S cistron tree. (b) Nuclear rDNA (45S) IGS tree. (c) Nuclear rDNA 5S tree. (d) Plastome tree. Mexico–Central–South American (MCSAI, MCSAII) and Mallopetalon groups are indicated by discontinuous-line rectangles. Ultrafast bootstrap support values are indicated on branches. Oryza sativa and Brachypodium distachyon outgroups were used to root the trees except for the IGS and 5S trees that were rooted at midpoint. Color codes of Loliinae lineages are indicated in the chart of (a). Scale bars: number of mutations per site.

Figure 3

(a) Histograms of repeat contents per holoploid genome (1C) retrieved from the individual Repeat Explorer 2 (RE2) analyses of the studied Mesoamerican and South American broad-leaved Festuca taxa and other Loliinae samples. Color codes for repeat types are indicated in the chart. (b) Phylogenetic network based on standardized repeat data sets retrieved from the comparative RE analysis and constructed from distance-based NJ trees computed with pairwise Euclidean distances between samples. Core BL, core FL, Schedonorus, Mexico–Central–South American (MCSAI, MCSAII), and Mallopetalon + other American Loliinae groups are surrounded by dashed lines. Color codes of Loliinae lineages are indicated in the chart.

Figure 3

(a) Histograms of repeat contents per holoploid genome (1C) retrieved from the individual Repeat Explorer 2 (RE2) analyses of the studied Mesoamerican and South American broad-leaved Festuca taxa and other Loliinae samples. Color codes for repeat types are indicated in the chart. (b) Phylogenetic network based on standardized repeat data sets retrieved from the comparative RE analysis and constructed from distance-based NJ trees computed with pairwise Euclidean distances between samples. Core BL, core FL, Schedonorus, Mexico–Central–South American (MCSAI, MCSAII), and Mallopetalon + other American Loliinae groups are surrounded by dashed lines. Color codes of Loliinae lineages are indicated in the chart.