The grass subfamily Pooideae: Cretaceous–Palaeocene origin and climate‐driven Cenozoic diversification

Abstract

Aim Frost is among the most dramatic stresses a plant can experience, and complex physiological adaptations are needed to endure long periods of sub‐zero temperatures. Owing to the need to evolve these complex adaptations, transitioning from tropical to temperate climates is regarded as difficult. Here, we study the transition from tropical to temperate climates in the grass subfamily Pooideae, which dominates cool temperate, continental and Arctic regions. We produce a dated phylogeny and investigate the role of climate cooling in diversification. Location Global, temperate regions. Time period Cretaceous–Cenozoic. Major taxa Pooideae. Methods Using newly available fossils and methods, we dated a comprehensive Pooideae phylogeny and tested for the impact of palaeoclimates on diversification rates. Using ancestral state reconstruction, we investigated whether Pooideae ancestors experienced frost and winter. To locate the ancestral distribution area of Pooideae, we performed biogeographical analyses. Results We estimated a Late Cretaceous/early Palaeocene origin of the Pooideae (61–77 Ma), with all major clades already having diversified at the Eocene–Oligocene climate cooling (34 Ma). Climate cooling was a probable driving force of Pooideae diversification. Pooideae probably evolved in a temperate niche experiencing frost, but not long winters. Main conclusion Pooideae probably originated in a temperate niche and experienced cold temperatures and frost long before expansion of temperate biomes after the Eocene–Oligocene transition. This suggests that the Pooideae ancestor had adaptations to temperate climate and that certain responses to low‐temperature stress are shared in extant Pooideae grasses. Throughout the Cenozoic, falling temperatures and expansion of temperate biomes were associated with an increase in diversification. However, complex mechanisms for enduring strongly seasonal climate with long, cold winters most probably evolved independently in daughter lineages. Our findings provide insight into how adaptations to historical changes in chill and frost exposure influence the distribution of plant diversity today.

Evolution of Cold Acclimation and Its Role in Niche Transition in the Temperate Grass Subfamily Pooideae

“…A, Schematic phylogeny of the study species. The species phylogeny and dates are inferred from Schubert et al (2018), except for B. sylvaticum, which was not included in the study. Placement and divergence date for B. sylvaticum are thus approximate.…”

“…Although Pooideae species dominate temperate and arctic grass floras (Hartley, 1973;Visser et al, 2014), the ancestors of this group were most likely adapted to tropical or subtropical climates (Bouchenak-Khelladi et al, 2010;Strömberg, 2011). Pooideae originated in the late Cretaceous or early Paleogene period (Bouchenak-Khelladi et al, 2010;Christin et al, 2014;Spriggs et al, 2014;Schubert et al, 2018) during a time where the global climate was generally warm (Zachos et al, 2001;Mudelsee et al, 2014) and seasonality in temperature was relatively low (Archibald et al, 2010). The colonization of temperate biomes by Pooideae was likely facilitated by the evolution of successful adaptations to cold conditions.…”

“…The colonization of temperate biomes by Pooideae was likely facilitated by the evolution of successful adaptations to cold conditions. Although studies have inferred adaptation to cooler environments at the base of the Pooideae phylogeny (Edwards and Smith, 2010;Schubert et al, 2018), it is still not known whether the Pooideae's most recent common ancestor already was adapted to cold and/or freezing conditions or if adaptations to cold evolved during the diversification of Pooideae along with falling temperatures throughout the Cenozoic and expansion of temperate biomes.…”

Increased above‐ground resource allocation is a likely precursor for independent evolutionary origins of annuality in the Pooideae grass subfamily

“…Model fit was determined based on AIC and log likelihood. Trees based on cpDNA regions (matK, ndhF, and rbcL) were obtained from the study of Schubert et al (2019). A sample of 1000 trees from the posterior distribution of a BEAST Markov Chain Monte Carlo (MCMC) analysis was used to test model adequacy for all four models in r8s (Sanderson, 2003).…”

“…Model fit parameters were summarised across the 1000 r8s runs for all models. From the same study of Schubert et al (2019), the timecalibrated ultrametric maximum clade credibility (MCC) tree was used to reconstruct ancestral states of annual life-cycle strategy. The precursor trait analyses in r8s are sensitive to tree size and trait distribution along its tips (Marazzi et al, 2012).…”