Global analysis of Poales diversification – parallel evolution in space and time into open and closed habitats

Abstract

● Poales are one of the most species-rich, ecologically and economically important orders of plants and often characterise open habitats, enabled by unique suites of traits. We test the hypotheses that Poales species are assembled into distinct phyloregions, with centres of high phylogenetic diversity and endemism clustered in tropical regions, and that cosmopolitan families show parallel transitions into open and closed habitats at different times. ● We sampled 42% of Poales species and obtained taxonomic and biogeographic data from the World Checklist of Vascular Plants database, which was combined with open/closed habitat data scored by taxonomic experts. A dated supertree of Poales was constructed. We integrated spatial phylogenetics with regionalization analyses, historical biogeography, ancestral state estimations, and models of contingent evolution. ● Diversification in Poales and assembly of open and closed habitats result from dynamic evolutionary processes that vary across lineages, time, space, and traits, most prominently in tropical and southern latitudes. Our results reveal parallel and recurrent patterns of habitat and trait transitions in the species-rich families Poaceae and Cyperaceae, yet other smaller families display unique evolutionary trajectories. ● The Poales have achieved global dominance via parallel evolution in open habitats, with notable, spatially and phylogenetically restricted divergences into strictly closed habitats.

Why plant diversity and distribution matter

“…Nevertheless, a multitude of traits other than climbing growth forms may be important for the evolutionary history, diversification and current distribution of plant species and lineagessuch as fruit size in palms (W€ olke et al, 2023) and the photosynthetic system in grasses (Elliott et al, 2023). Such effects of traits on diversity are context-specific; that is, they depend on the environmental setting in which diversification took place, such as Africa for large fruits (W€ olke et al, 2023), Central American rainforests for orchids (P erez-Escobar et al, 2023), temperature for the evolution of annual strategies in flowering plants (Boyko et al, 2023) and mid-Eocene conditions for the diversification and geographic expansion of Scrophulariaceae (Villaverde et al, 2023).…”

Drought tolerance as an evolutionary precursor to frost and winter tolerance in grasses

“…The two successive sisters to the rest sampled here ( Puelia olyriformis and Pharus latifolius ) are not part of any labelled subfamily or clade. Arrows indicate ancestral nodes where transitions from closed to open habitats may have occurred (Kellogg 2001; Bouchenak-Khelladi et al 2010; Zhang et al 2022; Elliott et al 2023).…”

“…Such habitats are today characteristic of a few small lineages that are successively sister to the rest of the family (Anomochloideae, Pharoideae and Puelloideae), the bamboos (Bambusoideae) and Brachyelytrum , which is sister to the rest of the Pooideae. However, the vast majority of grasses today occupy open environments (Elliott et al, 2023).…”

“…Transitions from closed to open environments are thought to have happened multiple times, certainly independently in the BOP and PACMAD clades, but exactly how many times and in which lineages is still unclear. Estimates range from one to as many as four independent transitions in the BOP clade, mainly in Pooideae, and one or possibly two in the PACMAD clade (Bouchenak-Khelladi et al, 2010; Elliott et al, 2023; Kellogg, 2001; Zhang et al, 2022). Both fossil and phylogenetic evidence suggests grasses began transitioning to open habitats around 67–58 Ma (Gallaher et al, 2019; Schubert, Marcussen, et al, 2019; Strömberg, 2011), at different times on different continents (Edwards et al, 2010; Strömberg, 2011).…”

“…Similarly, grasses have transitioned from tropical to temperate climates multiple times independently, most notably leading to the radiation of two distantly related lineages into cool temperate zones, the Pooideae and Danthonioideae. However, frost tolerance has never been reconstructed as deeply as the nodes at which transitions to open habitats are implied (Edwards & Smith, 2010; Elliott et al, 2023; Humphreys & Linder, 2013; Linder et al, 2018; Sandve & Fjellheim, 2010; Schubert, Grønvold, et al, 2019). This suggests that grasses adapted to aridity before cold and frost and sets up predictions for which clades may have been predisposed to adapting to low temperatures under the hypothesis tested here.…”