Phylogenomic and ecological analyses reveal the spatiotemporal evolution of global pines.

How coniferous forests evolved in the Northern Hemisphere remains largely unknown. Unlike most groups of organisms that generally follow a latitudinal diversity gradient, most conifer species in the Northern Hemisphere are distributed in mountainous areas at middle latitudes. It is of great interest to know whether the midlatitude region has been an evolutionary cradle or museum for conifers and how evolutionary and ecological factors have driven their spatiotemporal evolution. Here, we investigated the macroevolution of Pinus, the largest conifer genus and characteristic of northern temperate coniferous forests, based on nearly complete species sampling. Using 1,662 genes from transcriptome sequences, we reconstructed a robust species phylogeny and reestimated divergence times of global pines. We found that ∼90% of extant pine species originated in the Miocene in sharp contrast to the ancient origin of Pinus, indicating a Neogene rediversification. Surprisingly, species at middle latitudes are much older than those at other latitudes. This finding, coupled with net diversification rate analysis, indicates that the midlatitude region has provided an evolutionary museum for global pines. Analyses of 31 environmental variables, together with a comparison of evolutionary rates of niche and phenotypic traits with a net diversification rate, found that topography played a primary role in pine diversification, and the aridity index was decisive for the niche rate shift. Moreover, fire has forced diversification and adaptive evolution of Pinus Our study highlights the importance of integrating phylogenomic and ecological approaches to address evolution of biological groups at the global scale.

Diversification into novel habitats in the Africa clade of Dioscorea (Dioscoreaceae): erect habit and elephant's foot tubers.

BACKGROUND: Dioscorea is a widely distributed and highly diversified genus in tropical regions where it is represented by ten main clades, one of which diversified exclusively in Africa. In southern Africa it is characterised by a distinct group of species with a pachycaul or "elephant's foot" structure that is partially to fully exposed above the substrate. In contrast to African representatives of the genus from other clades, occurring mainly in forest or woodland, the pachycaul taxa and their southern African relatives occur in diverse habitats ranging from woodland to open vegetation. Here we investigate patterns of diversification in the African clade, time of transition from forest to more open habitat, and morphological traits associated with each habitat and evaluate if such transitions have led to modification of reproductive organs and mode of dispersal. RESULTS: The Africa clade originated in the Oligocene and comprises four subclades. The Dioscorea buchananii subclade (southeastern tropical Africa and South Africa) is sister to the East African subclade, which is respectively sister to the recently evolved sister South African (e. g., Cape and Pachycaul) subclades. The Cape and Pachycaul subclades diversified in the east of the Cape Peninsula in the mid Miocene, in an area with complex geomorphology and climate, where the fynbos, thicket, succulent karoo and forest biomes meet. CONCLUSIONS: Diversification out of forest is associated with major shifts in morphology of the perennial tuber (specifically an increase in size and orientation which presumably led them to become pachycaul) and rotation of stem (from twining to non-twining). The iconic elephant's foot morphology, observed in grasslands and thicket biomes, where its corky bark may offer protection against fire and herbivory, evolved since mid Miocene. A shift in pollination trait is observed within the forest, but entry into open habitat does not show association with reproductive morphology, except in the seed wing, which has switched from winged all round the seed margin to just at the base or at the apex of it, or has been even replaced by an elaiosome.

Savanna fire and the origins of the 'underground forests' of Africa.

The origin of fire-adapted lineages is a long-standing question in ecology. Although phylogeny can provide a significant contribution to the ongoing debate, its use has been precluded by the lack of comprehensive DNA data. Here, we focus on the 'underground trees' (=geoxyles) of southern Africa, one of the most distinctive growth forms characteristic of fire-prone savannas. We placed geoxyles within the most comprehensive dated phylogeny for the regional flora comprising over 1400 woody species. Using this phylogeny, we tested whether African geoxyles evolved concomitantly with those of the South American cerrado and used their phylogenetic position to date the appearance of humid savannas. We found multiple independent origins of the geoxyle life-form mostly from the Pliocene, a period consistent with the origin of cerrado, with the majority of divergences occurring within the last 2 million yr. When contrasted with their tree relatives, geoxyles occur in regions characterized by higher rainfall and greater fire frequency. Our results indicate that the geoxylic growth form may have evolved in response to the interactive effects of frequent fires and high precipitation. As such, geoxyles may be regarded as markers of fire-maintained savannas occurring in climates suitable for forests.

Some like it hot: Seed thermal threshold variation in obligate seeding Acacia pulchella along a climate gradient.

Dormancy in seeds is a key persistence mechanism for many flowering plants. Physically dormant (PY) seeds have water impermeable seed coats, and in fire-prone systems a common mechanism for dormancy release is fire-induced soil heating. However, the thermal thresholds innate to seeds with PY may be influenced by vegetation, climate, and fire regimes, varying substantially between populations of the same species. To investigate intraspecific variation of thermal thresholds in PY seeds, we sampled obligate seeding Acacia pulchella (Fabaceae) which produces PY seeds. Sampling was undertaken from 13 populations across a climate gradient of rainfall and temperature, and between two vegetation communities in fire-prone Mediterranean-type ecosystems of south-west Western Australia. To test a range of weather and fire-induced soil heating dormancy-break scenarios, we conducted dry heat shock experiments between 40 and 140 °C for 10 min and scored germination for 16 weeks. We created population-specific thermal performance curves and extracted the dormancy release temperature at which 50 % of the seeds had germinated (DRT50), the optimum dormancy-breaking temperature to stimulate maximum germination (T0), and the lethal temperature at which 50 % of the seeds were killed (LT50). Generalised linear models were used to examine relationships between thermal thresholds and possible vegetation, climate, and fire regime drivers of intraspecific variation in seed traits. We found that thermal thresholds differed between vegetation communities, with thresholds consistently higher in forest-type ecosystems compared to open woodland, and the influence of climate varied significantly between the two communities. Seeds from Jarrah Forest populations had a DRT50 16.0 °C higher, a T0 9.7 °C higher, and LT50 7.8 °C higher than seeds from Banksia woodlands. A high rate of non-dormancy was identified in one population that had lost fire in its system and displayed significant germination after both summer and fire-related temperatures. The PY thermal thresholds modelled here provide insight into the strong influence of variable soil heating as a function of vegetation and fuel dynamics in fire-prone environments. Our findings highlight the significant intraspecific variation for this species and suggest that fire-induced soil heating generated by vegetation characteristics may be an overlooked element of fire regimes shaping seed traits.

Burning lignin: overlooked cues for post-fire seed germination.

Information about smoke cues for seed germination is fundamental to understanding fire adaptation. Recently, lignin-derived syringaldehyde (SAL) was identified as a new smoke cue for seed germination, which challenges the assumption that cellulose-derived karrikins are the primary smoke cues. We highlight the overlooked association between lignin and the fire adaptation of plants.

What drives grassland-forest boundaries? Assessing fire and frost effects on tree seedling survival and architecture.

Fire and frost represent two major hurdles for the persistence of trees in open grassy biomes and have both been proposed as drivers of grassland-forest boundaries in Africa.We assess the response of young tree seedlings, which represent a vulnerable stage in tree recruitment, to traumatic fire and frost disturbances.In a greenhouse experiment, we investigated how seedling traits predicted survival and resprouting ability in response to fire versus frost; we characterized survival strategies of seedlings in response to the two disturbances, and we documented how the architecture of surviving seedlings is affected by fire versus frost injury.Survival rates were similar under both treatments. However, different species displayed different levels of sensitivity to fire and frost. Seedling survival was higher for older seedlings and seedlings with more basal leaves. Survivors of a fire event lost more biomass than the survivors of a frost event. However, the architecture of recovered fire- and frost-treated seedlings was mostly similar. Seedlings that recovered from fire and frost treatments were often shorter than those that had not been exposed to any disturbance, with multiple thin branches, which may increase vulnerability to the next frost or fire event. Synthesis. Fire caused more severe aboveground damage compared with a single frost event, suggesting that fire is an important driver of tree distribution in these open grassland systems. However, the impact of repeated frost events may be equally severe and needs to be investigated. Also, woody species composition may be influenced by phenomena that affect the timing and frequency of seedling exposure to damage, as mortality was found to be dependent on seedling age. Therefore, changes in fire regime and climate are likely to result in changes in the composition and the structure of the woody components of these systems.

How Does Water Availability Affect the Allocation to Bark in a Mediterranean Conifer?

Bark thickness is a key structural feature in woody plants in the protection against fire. We used 19 provenances of Pinus halepensis, an obligate-seeder species, in a replicated common garden at two environments contrasting in water availability to assess the interacting effects of site environment and population in the relative allocation to bark, expecting lower allocation at the drier site. Secondly, given the average fire frequency, we analyzed whether trees reached the critical absolute thickness soon enough for population persistence via aerial seed bank. Our analyses indicated that trees at the moister site allocated a rather fixed quantity of resources independent of tree size, and almost all populations reached critical absolute bark thickness to eventually survive fire. In contrast, at the drier site allocation to bark reduced with tree size, and most populations did not reach the critical bark thickness. Populations from areas with higher fire frequency had thicker basal bark, while those from areas with severe droughts and short vegetative periods, had thinner bark. In conclusion, drought-stressed trees have a higher risk to die from fires before achieving reproduction and building a sufficient aerial seed bank.

Fire-Proneness as a Prerequisite for the Evolution of Fire-Adapted Traits.

Fire as a major evolutionary force has been disputed because it is considered to lack supporting evidence. If a trait has evolved in response to selection by fire then the environment of the plant must have been fire-prone before the appearance of that trait. Using outcomes of trait assignments applied to molecular phylogenies for fire-stimulated flowering, seed-release, and germination, in this Opinion article we show that fire-proneness precedes, or rarely coincides with, the evolution of these fire-adapted traits. In addition, fire remains central to understanding germination promoted by smoke among species occurring in non-fire-prone environments because of the historical association of their clade with fire. Fire-mimicking selection and associated exaptations have no place in understanding the evolution of fire-adapted traits because we find no support for any reversal in the fire-trait sequence through time.

Temperature thresholds of physically dormant seeds and plant functional response to fire: variation among species and relative impact of climate change.

Variation in dormancy thresholds among species is rarely studied but may provide a basis to better understand the mechanisms controlling population persistence. Incorporating dormancy-breaking temperature thresholds into existing trait frameworks could improve predictions regarding seed bank persistence, and subsequently species resilience in response to fire, climate change and anthropogenic management. A key ecological strategy for many species from fire-prone ecosystems is the possession of a long-lived seed bank, ensuring recovery after fire. Physical dormancy is dominant in these ecosystems and maintaining this dormancy is directly linked to seed bank persistence. We identified a suite of seed-related factors relevant to maintaining populations in fire-prone regions for 14 co-occurring physically dormant species. We measured variation in initial levels of dormancy and then applied experimental heating treatments, based on current seasonal temperatures and those occurring during fires, to seeds of all study species. Additionally, higher seasonal temperature treatments were applied to assess response of seeds to temperatures projected under future climate scenarios. Levels of germination response and mortality were determined to assess how tightly germination response was bound to either fire or seasonal cues. Six species were found to have dormancy cues bound to temperatures that only occur during fires (80°C and above) and were grouped as having obligate pyrogenic dormancy release. The remaining species, classified as having facultative pyrogenic dormancy, had lower temperature dormancy thresholds and committed at least 30% of seeds to germinate after summer-temperature treatments. Evidence from this study supports including dormancy-breaking temperature thresholds as an attribute for identifying functional types. High temperature thresholds for breaking dormancy, found in our obligate pyrogenic group, appear to be a fire-adapted trait, while we predict that species in the facultative group are most at risk to increased seed bank decay resulting from elevated soil temperatures under projected climate change.