Hybridisation and chloroplast capture between distinct Themeda triandra lineages in Australia

Abstract

Ecotypes are distinct populations within a species that are adapted to specific environmental conditions. Understanding how these ecotypes become established, and how they interact when reunited, is fundamental to elucidating how ecological adaptations are maintained. This study focuses on Themeda triandra, a dominant grassland species across Asia, Africa and Australia. It is the most widespread plant in Australia, where it has distinct ecotypes that are usually restricted to either wetter and cooler coastal regions or the drier and hotter interior. We generate a reference genome for T. triandra and use whole genome sequencing for over 80 Themeda accessions to reconstruct the evolutionary history of T. triandra and related taxa. Organelle phylogenies confirm that Australia was colonized by T. triandra twice, with the division between ecotypes predating their arrival in Australia. The nuclear genome provides evidence of differences in the dominant ploidal level and gene-flow among the ecotypes. In northern Queensland there appears to be a hybrid zone between ecotypes with admixed nuclear genomes and shared chloroplast haplotypes. Conversely, in the cracking claypans of Western Australia, there is cytonuclear discordance with individuals possessing the coastal chloroplast and interior clade nuclear genome. This chloroplast capture is potentially a result of adaptive introgression, with selection detected in the rpoC2 gene which is associated with water use efficiency. The reason that T. triandra is the most widespread plant in Australia appears to be a result of distinct ecotypic genetic variation and genome duplication, with the importance of each depending on the geographic scale considered.

Keywords: adaptation; andropogoneae; angiosperms; ecological genetics; phylogeography; population genetics.

FIGURE 1

Phylogenetic relationships of Themeda inferred from whole (a) chloroplast (inverted repeat removed) and (b) mitochondrial genomes. In both cases, the maximum likelihood topology with bootstrap support values are shown, inferred with the (a) GTR + I + G and (b) TVM + F + R2 substitution model. For samples not assigned to a clade, a three letter abbreviation is used (THA, Thailand; PHI, Philippines; TAN, Tanzania; CHN, China; AUS, Australia). The asterisks indicate samples for which only chloroplast genomes are available. Truncated branches are indicated. (c) the sampling locations of T. triandra accessions in Australia clade I and II are shown, with potential hybrids from northern Queensland indicated.

FIGURE 2

Phylogenetic relationships of Themeda inferred from 2096 nuclear genes. (a) a maximum likelihood topology from a concatenated alignment of all loci with colours of the Australian clades based on chloroplast groupings (Figure 1). Bootstrap support values for the concatenated maximum likelihood tree are shown, followed by local posterior probabilities from a coalescence species tree for the same nuclear loci. The pie charts on key nodes represent the individual gene tree support for the topology shown. (b) a densitree plot of overlaid nuclear gene trees. Colours match the chloroplast clades, and truncated branches are indicated. For samples not assigned to a clade a three letter abbreviation is used (PHI = Philippines and CHN = China), and the clade containing potential hybrids from northern Queensland (nQ) is indicated.

FIGURE 3

Nuclear genetic variation and structure within Themeda. (a) a principal component analysis across the first two axes is shown, with genetic groups coloured based on the chloroplast phylogeny shown in Figure 1. (b) the mean likelihood and standard error for a range of K's is shown, with these values used to calculate ΔK (c) as in Evanno et al. (2005). (d) the assignment to genetic clusters is shown for two values of K. samples are arranged within their chloroplast clade (indicated by that bar underneath the admixture plots), and ordered from west to east within each group. The asterisks indicate samples with a high degree of admixture from northern Queensland, and accessions from the Philippines (PHI) and China (CHN) are also indicated on the admixture plot.

FIGURE 4

Distribution of F _ST between the three Australian Themeda triandra ecotypes/clades considered in this study (coastal, inland and claypan). (a) F _ST values were calculated along the 10 chromosomes in 50 kb windows (10 kb slide), with the red line indicating the mean F _ST value. (b) a violin plot summarizes the F _ST values for each comparison with mean and standard deviation shown.