Global variation in the thermal tolerances of plants.

Thermal macrophysiology is an established research field that has led to well-described patterns in the global structuring of climate adaptation and risk. However, since it was developed primarily in animals, we lack information on how general these patterns are across organisms. This is alarming if we are to understand how thermal tolerances are distributed globally, improve predictions of climate change, and mitigate effects. We approached this knowledge gap by compiling a geographically and taxonomically extensive database on plant heat and cold tolerances and used this dataset to test for thermal macrophysiological patterns and processes in plants. We found support for several expected patterns: Cold tolerances are more variable and exhibit steeper latitudinal clines and stronger relationships with local environmental temperatures than heat tolerances overall. Next, we disentangled the importance of local environments and evolutionary and biogeographic histories in generating these patterns. We found that all three processes have significantly contributed to variation in both heat and cold tolerances but that their relative importance differs. We also show that failure to simultaneously account for all three effects overestimates the importance of the included variable, challenging previous conclusions drawn from less comprehensive models. Our results are consistent with rare evolutionary innovations in cold acclimation ability structuring plant distributions across biomes. In contrast, plant heat tolerances vary mainly as a result of biogeographical processes and drift. Our results further highlight that all plants, particularly at mid-to-high latitudes and in their nonhardened state, will become increasingly vulnerable to ongoing climate change.

The evolutionary reality of species and higher taxa in plants: a survey of post-modern opinion and evidence.

Species are normally considered to be the fundamental unit for understanding the evolution of biodiversity. Yet, in a survey of botanists in 1940, twice as many felt that plant genera were more natural units than plant species. Revisiting the survey, we found more people now regarded species as a more evolutionarily real unit, but a sizeable number still felt that genera were more evolutionarily real than species. Definitions of 'evolutionarily real' split into those based on shared evolutionary history and those based on shared evolutionary fate via ongoing evolutionary processes. We discuss recent work testing for shared evolutionary fate at the species and higher levels and present preliminary evidence for evolutionarily significant higher taxa in plants.

The evolutionary reality of higher taxa in mammals.

Species are generally regarded as a fundamental unit of biodiversity. By contrast, higher taxa such as genera and families, while widely used as biodiversity metrics and for classification and communication, are generally not believed to be shaped by shared evolutionary processes in the same way as species. We use simulations to show that processes which are important for emergence of evolutionarily significant units (ESUs) at the species level, namely geographical isolation and ecological divergence, can generate evolutionary independence above the species level and thereby lead to emergence of discrete phylogenetic clusters (higher ESUs). Extending phylogenetic approaches for delimiting evolutionarily significant species to broader phylogenetic scales, we find evidence for the existence of higher ESUs in mammals. In carnivores, euungulates and lagomorphs the hierarchical level of units detected correspond, on average, to the level of family or genus in traditional taxonomy. The units in euungulates are associated with divergent patterns of body mass, consistent with occupation of distinct ecological zones. Our findings demonstrate a new framework for studying biodiversity that unifies approaches at species and higher levels, thus potentially restoring higher taxa to their historical status as natural entities.

Evidence for recent evolution of cold tolerance in grasses suggests current distribution is not limited by (low) temperature.

· Temperature is considered an important determinant of biodiversity distribution patterns. Grasses (Poaceae) occupy among the warmest and coldest environments on earth but the role of cold tolerance evolution in generating this distribution is understudied. We studied cold tolerance of Danthonioideae (c. 280 species), a major constituent of the austral temperate grass flora. · We determined differences in cold tolerance among species from different continents grown in a common winter garden and assessed the relationship between measured cold tolerance and that predicted by species ranges. We then used temperatures in current ranges and a phylogeny of 81% of the species to study the timing and mode of cold tolerance evolution across the subfamily. · Species ranges generally underestimate cold tolerance but are still a meaningful representation of differences in cold tolerance among species. We infer cold tolerance evolution to have commenced at the onset of danthonioid diversification, subsequently increasing in both pace and extent in certain lineages. Interspecific variation in cold tolerance is better accounted for by spatial than phylogenetic distance. · Contrary to expectations, temperature - low temperature in particular - appears not to limit the distribution of this temperate clade. Competition, time or dispersal limitation could explain its relative absence from northern temperate regions.

Convergent evolution of the annual life history syndrome from perennial ancestors.

Despite most angiosperms being perennial, once-flowering annuals have evolved multiple times independently, making life history traits among the most labile trait syndromes in flowering plants. Much research has focused on discerning the adaptive forces driving the evolution of annual species, and in pinpointing traits that distinguish them from perennials. By contrast, little is known about how 'annual traits' evolve, and whether the same traits and genes have evolved in parallel to affect independent origins of the annual syndrome. Here, we review what is known about the distribution of annuals in both phylogenetic and environmental space and assess the evidence for parallel evolution of annuality through similar physiological, developmental, and/or genetic mechanisms. We then use temperate grasses as a case study for modeling the evolution of annuality and suggest future directions for understanding annual-perennial transitions in other groups of plants. Understanding how convergent life history traits evolve can help predict species responses to climate change and allows transfer of knowledge between model and agriculturally important species.

Absence of mammals and the evolution of New Zealand grasses.

Anthropogenic alteration of biotic distributions and disturbance regimes has dramatically changed the evolutionary context for the differentiation of species traits. Some of the most striking examples in recent centuries have been on islands where flightless birds, which evolved in the absence of mammalian carnivores, have been decimated following the widespread introduction of exotic predators. Until now, no equivalent case has been reported for plants. Here, we make use of robust analytical tools and an exceptionally well-sampled molecular phylogeny to show that a majority of New Zealand danthonioid grasses (Poaceae) may have adapted to the relaxed vertebrate herbivore pressure during the late Cenozoic through the development of a distinctive and unusual habit: abscission of old leaves. This feature occurs in only about 3 per cent of the world's roughly 11,000 grass species and has been empirically shown to increase plant productivity but to reduce protection against mammal grazing. This result suggests that release from a selective pressure can lead to species radiations. This seemingly anachronistic adaptation may represent an overlooked factor contributing to the severe decline in the geographical extent and species diversity of New Zealand's indigenous grasslands following the introduction of herbivorous terrestrial mammals in the 19th century.

A plastid tree can bring order to the chaotic generic taxonomy of Rytidosperma Steud. s.l. (Poaceae).

Rytidosperma s.l., wallaby grasses and allies, is in dire need of a single, unanimously accepted generic taxonomy. Motivated by the desire to establish a generic classification that complies with phylogeny, we investigated how much phylogenetic signal is contained within a plastid (cpDNA) tree, given that the nrDNA tree (ITS) was uninformative and that a phylogenetic hypothesis based on a single genome may not be reliable. We find that the plastid tree is significantly different from a morphological cladogram and show that this is the result of homoplasy in the morphological dataset. Treated individually, several morphological characters fit the plastid tree very well. Similarly, we find a good fit of the plastid tree with ecological and distribution characters and with biogeographical patterns in the Southern Hemisphere. We conclude that a significant level of the species phylogeny is resolved by the plastid tree and are confident it can form a sound basis for a reconsideration of generic limits. None of the currently recognised seven genera in the Rytidosperma clade is monophyletic. Therefore, we propose combining the segregate genera in Australasia within a broadly construed Rytidosperma, including all the species from Australia, New Guinea, New Zealand and South America.

Reticulation, data combination, and inferring evolutionary history: an example from Danthonioideae (Poaceae).

We explore the potential impact of conflicting gene trees on inferences of evolutionary history above the species level. When conflict between gene trees is discovered, it is common practice either to analyze the data separately or to combine the data having excluded the conflicting taxa or data partitions for those taxa (which are then recoded as missing). We demonstrate an alternative approach, which involves duplicating conflicting taxa in the matrix, such that each duplicate is represented by one partition only. This allows the combination of all available data in standard phylogenetic analyses, despite reticulations. We show how interpretation of contradictory gene trees can lead to conflicting inferences of both morphological evolution and biogeographic history, using the example of the pampas grasses, Cortaderia. The characteristic morphological syndrome of Cortaderia can be inferred as having arisen multiple times (chloroplast DNA [cpDNA]) or just once (nuclear ribosomal DNA [nrDNA]). The distributions of species of Cortaderia and related genera in Australia/New Guinea, New Zealand, and South America can be explained by few (nrDNA) or several (cpDNA) dispersals between the southern continents. These contradictions can be explained by past hybridization events, which have linked gains of complex morphologies with unrelated chloroplast lineages and have erased evidence of dispersals from the nuclear genome. Given the discrepancies between inferences based on the gene trees individually, we urge the use of approaches such as ours that take multiple gene trees into account.

Global dataset shows geography and life form predict modern plant extinction and rediscovery.

Most people can name a mammal or bird that has become extinct in recent centuries, but few can name a recently extinct plant. We present a comprehensive, global analysis of modern extinction in plants. Almost 600 species have become extinct, at a higher rate than background extinction, but almost as many have been erroneously declared extinct and then been rediscovered. Reports of extinction on islands, in the tropics and of shrubs, trees or species with narrow ranges are least likely to be refuted by rediscovery. Plant extinctions endanger other organisms, ecosystems and human well-being, and must be understood for effective conservation planning.

A novel supermatrix approach improves resolution of phylogenetic relationships in a comprehensive sample of danthonioid grasses.

Phylogeny reconstruction is challenging when branch lengths vary and when different genetic loci show conflicting signals. The number of DNA sequence characters required to obtain robust support for all the nodes in a phylogeny becomes greater with denser taxon sampling. We test the usefulness of an approach mixing densely sampled, variable non-coding sequences (trnL-F; rpl16; atpB-rbcL; ITS) with sparsely sampled, more conservative protein coding and ribosomal sequences (matK; ndhF; rbcL; 26S), for the grass subfamily Danthonioideae. Previous phylogenetic studies of Danthonioideae revealed extensive generic paraphyly, but were often impeded by insufficient character and taxon sampling and apparent inter-gene conflict. Our variably-sampled supermatrix approach allowed us to represent 79% of the species with up to c. 9900 base pairs for taxa representing the major clades. A 'taxon duplication' approach for taxa with conflicting phylogenetic signals allowed us to combine the data whilst representing the differences between chloroplast and nuclear encoded gene trees. This approach efficiently improves resolution and support whilst maximising representation of taxa and their sometimes composite evolutionary histories, resulting in a phylogeny of the Danthonioideae that will be useful both for a wide range of evolutionary studies and to inform forthcoming realignment of generic delimitations in the subfamily.

Effects of phylogenetic reconstruction method on the robustness of species delimitation using single-locus data.

Coalescent-based species delimitation methods combine population genetic and phylogenetic theory to provide an objective means for delineating evolutionarily significant units of diversity. The generalised mixed Yule coalescent (GMYC) and the Poisson tree process (PTP) are methods that use ultrametric (GMYC or PTP) or non-ultrametric (PTP) gene trees as input, intended for use mostly with single-locus data such as DNA barcodes. Here, we assess how robust the GMYC and PTP are to different phylogenetic reconstruction and branch smoothing methods. We reconstruct over 400 ultrametric trees using up to 30 different combinations of phylogenetic and smoothing methods and perform over 2000 separate species delimitation analyses across 16 empirical data sets. We then assess how variable diversity estimates are, in terms of richness and identity, with respect to species delimitation, phylogenetic and smoothing methods. The PTP method generally generates diversity estimates that are more robust to different phylogenetic methods. The GMYC is more sensitive, but provides consistent estimates for BEAST trees. The lower consistency of GMYC estimates is likely a result of differences among gene trees introduced by the smoothing step. Unresolved nodes (real anomalies or methodological artefacts) affect both GMYC and PTP estimates, but have a greater effect on GMYC estimates. Branch smoothing is a difficult step and perhaps an underappreciated source of bias that may be widespread among studies of diversity and diversification. Nevertheless, careful choice of phylogenetic method does produce equivalent PTP and GMYC diversity estimates. We recommend simultaneous use of the PTP model with any model-based gene tree (e.g. RAxML) and GMYC approaches with BEAST trees for obtaining species hypotheses.

Ecology and evolution of the diaspore "burial syndrome".

Hygroscopically active awns or "bristles" have long intrigued scientists. Experimental evidence shows that they are important for diaspore burial in the correct orientation, thereby increasing successful seed germination and seedling survival. Despite these ecological advantages, 38 of the 280 species of grasses in Danthonioideae lack awns. We provide the first study of awns in a phylogenetic context and show that although the awnless state has arisen ca. 25 times independently, the ecological disadvantage of not having an awn also applies in an evolutionary context. Only in Tribolium and Schismus have awnless ancestors diversified to form a clade of primarily awnless descendents. Several of the awnless species in these genera are annual and we find a significant correlation between the evolution of awns and the evolution of life history. A suite of other diaspore traits accompany the awned or awnless states. We interpret the awn as being the visible constituent of a compound "burial syndrome," the two ecological extremes of which may explain the correlation between awns and life history and provide an explanation why awnless species in Tribolium and Schismus persist.