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 six hypotheses regarding the evolution and assembly of Poales in open and closed habitats throughout the world, and examine whether diversification patterns demonstrate parallel evolution. 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 regionalisation analyses, historical biogeography and ancestral state estimations. Diversification in Poales and assembly of open and closed habitats result from dynamic evolutionary processes that vary across lineages, time and space, 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. Smaller families display unique and often divergent 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.

Keywords: biogeography; evolution; evolutionary transitions; grasslands; grass‐like plants; savannas; spatial phylogenetics.

Fig. 1

Representatives of 12 Poales families. (a) Tillandsia tovarensis (Bromeliaceae), epiphytic in cloud forest, Kuelap, N Peru. (b) Insect‐pollinated Rhynchospora colorata (Cyperaceae), in forest gaps, S Ecuador. (c) Ecdeiocolea rigens (Ecdeiocoleaceae), arid heath, SW Australia. (d) Paepalanthus ensifolius (Eriocaulaceae), in cloud forest, Podocarpus National Park, S Ecuador. (e) Flagellaria indica (Flagellariaceae), rocky savannah, NW Australia. (f) Mayaca fluviatilis (Mayacaceae), wetlands, Singapore. (g) Micraira sp. Purnululu (Poaceae), a rapid‐resurrection species from sandstone pavements in NW Australia. (h) Guacamaya superba (Rapataceae) in a sedge and grass swamp in E Colombia. (i) Lepidobolus preissii (Restionaceae) from sandy heath, SW Australia. (j) Prionium serratum (Thurniaceae) in fynbos, Cape Province, South Africa. (k) Sparganium japonicum (Typhaceae) from wetlands in E Russia. (l) Xyris complanata (Xyridaceae) from an ephemeral wetland in savannah, NW Australia. Photos by Russell Barrett; except for (f, h, j, k), all posted on iNaturalist as CC‐BY‐NC; (f) by CheongWeei Gan; (h) by Carlos Eduardo; (j) by Linda Hibbin; (k) by Sergei Prokopenko.

Fig. 2

Global phylogenetic patterns of regionalisation in Poales. ( a) Phylogenetic regionalisation of the six largest families of Poales. Graphs represent the logarithmic species richness of the six families through time within each of the 13 phyloregions identified using the elbow and K‐means approach, where dotted lines represent open habitat lineages and solid lines indicate closed habitat lineages. A geological timeline is located in the inset in the far left‐hand corner, with the following abbreviations: Cretaceous (C: 66–56 Myr); Paleocene (P: 66–56 Myr); Eocene (E: 56–33.9 Myr); Oligocene (O: 33.9–23 Myr) and Miocene (M: 23–5.3 Myr). Inset to the right of the geological timeline shows nestedness of the 13 regions based on non‐metric multidimensional scaling (NMDS), where each colour dot represent a phyloregion and the three clusters each with similar colour dots represent the three major botanical kingdoms (Temperate, Neotropics, Palaeotropics). (b) Phylogenetic diversity (PD) of the six most speciose families of Poales, with red and dark blue indicating botanical countries with relatively high and low PD values, respectively. Botanical regions indicated by grey in (b) lack species for the respective family.

Fig. 3

Ancestral area reconstruction within Poales based on seven regions, obtained using the dispersal–extinction–cladogenesis (DEC) model in BioGeoBEARS (a). A global map showing colours corresponding to the seven defined areas for the BioGeoBEARS analysis is in the centre of the phylogenetic reconstruction. The crown nodes of the families within Poales are shown with black circles, whereas dark grey squares are used to depict lineages important for the study's interpretations. Concentric light grey/white rings underlying the phylogeny indicate time slots of 20 Myr intervals. Note that Joinvilleaceae and Ecdeiocoleaceae are depicted together for visual purposes. Number of dispersal events between the seven regions inferred using Biogeographical Stochastic Mapping on the DEC model (b), and (c) number of transitions between open and closed habitats inferred to have occurred within each of the seven areas, calculated through comparison of best fitting corHMM models and historical biogeographical estimates. The colours of row and column labels in (b) and row in (c) correspond to those on inset map in (a).

Fig. 4

Ancestral states of open/closed habitats based on Generalized Hidden Markov models, with hidden rates model with two categories and asymmetric rates, implemented with the corHMM package in R. The crown nodes of the families within Poales are shown with black circles, whereas dark grey squares are used to depict lineages important for the study's interpretations. Concentric light grey/white rings underlying the phylogeny indicate time slots of 20 Myr intervals. Detailed transition rates between the states and rate are given in Table S5.

Fig. 5

Biodiversity patterns in Poales represented by Faith's phylogenetic diversity (PD) for open habitat species (a) and PD for closed habitat species (b); (c) Rosauer's phylogenetic endemism (PE) and (d) PE significance; and (e) centres of palaeo‐ and neo‐endemism determined using CANAPE for all Poales (left) and the six most speciose families (right). High PE significance indicates that the region has an overrepresentation of short, rare branches. Low PE significance indicates that short, rare branches are underrepresented. ns, not significant.