Evolution of genome size and GC content in the tribe Carduinae (Asteraceae): rare descending dysploidy and polyploidy, limited environmental control and strong phylogenetic signal

Genome size and GC content are basic species-specific attributes often delimiting genera or higher taxa, which enable the identification of polyploidy, hybridization and other modes of genome or karyotype evolution. The evolution of these genomic traits can often occur as a result of the selective pressure of the environment. Here, we reconstruct the evolution of these genomic traits in subtribe Carduinae (Asteraceae) in the context of changes in chromosome numbers. Using flow cytometry, genome size and GC content were estimated for 119 taxa and mapped onto a phylogenetic tree constructed using sequences from seven genetic markers. In addition, the genomic data were compared with the length of stomatal guard cells and achene size (length, weight) to evaluate the extent to which genomic characters could evolve adaptively in this subtribe. We found strong phylogenetic signals for the analysed genomic and phenotypic traits, which delimited most Carduinae genera or clades in agreement with the reconstructed phylogeny. Monoploid genome size was positively correlated with genomic GC content and stomatal guard cell length. In Cirsium, whose species were the focus of the majority of the analyses, the large-genomed subgen. Lophiolepis had smaller guard cells, which might be related to it occurring in more xeric habitats compared to subgen. Cirsium. In contrast, the achenes of the large-genomed subgen. Lophiolepis were larger, possibly in response to the summer drought, whereas achene weight and length were independent of genome size across the subtribe. Thus, genome size in the subtribe Carduinae might evolve under weak environmental control, at least under that mediated by the size of guard cells or achenes. Achene size was related positively to GC content, which could have evolved adaptively in response to summer drought. In Carduus and the North American Cirsium taxa, there is an increase in average chromosome size with reduction in monoploid chromosome number, suggesting descending dysploidy associated with chromosomal fusion. Polyploidy is relatively rare in this subtribe and was confirmed only in five of the species studied, including Cirsium vulgare, an invasive species that likely originated via distant (intersubgeneric) hybridization, as suggested by its intermediate genomic and achene features combined with the conflict between its morphology and phylogenetic position. Phylogenetic reconstruction, differences in genomic parameters, as well as stomatal guard cell and achene sizes support the separation of a monophyletic Lophiolepis from the remainder of Cirsium. Genome and achene size results also indicate that the early diverging Cirsium italicum can be separated from the rest of the monophyletic Lophiolepis+Picnomon+Notobasis clade.