Angiosperms have become the dominant terrestrial plant group by diversifying for~145 million years into a broad range of environments. During the course of evolution, numerous morphological innovations arose, often preceded by whole genome duplications (WGD). The mustard family (Brassicaceae), a successful angiosperm clade with~4000 species, has been diversifying into many evolutionary lineages for more than 30 million years. Here we develop a species inventory, analyze morphological variation, and present a maternal, plastome-based genus-level phylogeny. We show that increased morphological disparity, despite an apparent absence of clade-specific morphological innovations, is found in tribes with WGDs or diversification rate shifts. Both are important processes in Brassicaceae, resulting in an overall high net diversification rate. Character states show frequent and independent gain and loss, and form varying combinations. Therefore, Brassicaceae pave the way to concepts of phylogenetic genome-wide association studies to analyze the evolution of morphological form and function.
Background and Aims
Whole-genome duplication (WGD) events are considered important driving forces of diversification. At least 11 out of 52 Brassicaceae tribes had independent mesopolyploid WGDs followed by diploidization processes. However, the association between mesopolyploidy and subsequent diversification is equivocal. Herein we show the results from a family-wide diversification analysis on Brassicaceae, and elaborate on the hypothesis that polyploidization per se is a fundamental driver in Brassicaceae evolution.
Methods
We established a time-calibrated chronogram based on whole plastid genomes comprising representative Brassicaceae taxa and published data spanning the entire Rosidae clade. This allowed us to set multiple calibration points and anchored various Brassicaceae taxa for subsequent downstream analyses. All major splits among Brassicaceae lineages were used in BEAST analyses of 48 individually analysed tribes comprising 2101 taxa in total using the internal transcribed spacers of nuclear ribosomal DNA. Diversification patterns were investigated on these tribe-wide chronograms using BAMM and were compared with family-wide data on genome size variation and species richness.
Key Results
Brassicaceae diverged 29.9 million years ago (Mya) during the Oligocene, and the majority of tribes started diversification in the Miocene with an average crown group age of about 12.5 Mya. This matches the cooling phase right after the Mid Miocene climatic optimum. Significant rate shifts were detected in 12 out of 52 tribes during the Mio- and Pliocene, decoupled from preceding mesopolyploid WGDs. Among the various factors analysed, the combined effect of tribal crown group age and net diversification rate (speciation minus extinction) is likely to explain sufficiently species richness across Brassicaceae tribes.
Conclusions
The onset of the evolutionary splits among tribes took place under cooler and drier conditions. Pleistocene glacial cycles may have contributed to the maintenance of high diversification rates. Rate shifts are not consistently associated with mesopolyploid WGD. We propose, therefore, that WGDs in general serve as a constant ‘pump’ for continuous and high species diversification.
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