Blocking then stinging as a case of two-step evolution of defensive cage architectures in herbivore-driven ecosystems.

Dense branching and spines are common features of plant species in ecosystems with high mammalian herbivory pressure. While dense branching and spines can inhibit herbivory independently, when combined, they form a powerful defensive cage architecture. However, how cage architecture evolved under mammalian pressure has remained unexplored. Here we show how dense branching and spines emerged during the age of mammalian radiation in the Combretaceae family and diversified in herbivore-driven ecosystems in the tropics. Phylogenetic comparative methods revealed that modern plant architectural strategies defending against large mammals evolved via a stepwise process. First, dense branching emerged under intermediate herbivory pressure, followed by the acquisition of spines that supported higher speciation rates under high herbivory pressure. Our study highlights the adaptive value of dense branching as part of a herbivore defence strategy and identifies large mammal herbivory as a major selective force shaping the whole plant architecture of woody plants.

Evolutionary radiation of the Eurasian Pinus species under pervasive gene flow.

Evolutionary radiation, a pivotal aspect of macroevolution, offers valuable insights into evolutionary processes. The genus Pinus is the largest genus in conifers with c . 90% of the extant species emerged in the Miocene, which signifies a case of rapid diversification. Despite this remarkable history, our understanding of the mechanisms driving radiation within this expansive genus has remained limited. Using exome capture sequencing and a fossil-calibrated phylogeny, we investigated the divergence history, niche diversification, and introgression among 13 closely related Eurasian species spanning climate zones from the tropics to the boreal Arctic. We detected complex introgression among lineages in subsection Pinus at all stages of the phylogeny. Despite this widespread gene exchange, each species maintained its genetic identity and showed clear niche differentiation. Demographic analysis unveiled distinct population histories among these species, which further influenced the nucleotide diversity and efficacy of purifying and positive selection in each species. Our findings suggest that radiation in the Eurasian pines was likely fueled by interspecific recombination and further reinforced by their adaptation to distinct environments. Our study highlights the constraints and opportunities for evolutionary change, and the expectations of future adaptation in response to environmental changes in different lineages.

Kin and Non-Kin Connected Plants Benefit More Than Disconnected Kin and Non-Kin Plants under Nutrient-Competitive Environments.

In the natural environment, plants grow and interact with both conspecific and heterospecific neighbours under different environmental conditions. In this study, we tested whether Chenopodium quinoa Willd genotypes differ in growth performance when grown with kin and non-kin under nutrient limitation in pot partitioning treatments. Biomass accumulation, allocation, organ efficiency, and specific leaf area were measured at the end of the experiment. Response variables were differentially impacted by kinship, fertility, and barrier. Total dry mass, shoot dry mass, and root and stem allocation were greater for plants grown with kin in connected pots than with non-kin in connected pots across the nutrient treatments. Kin connected and disconnected plants had a greater specific root length, specific stem length, and average leaf mass than non-kin connected and disconnected plants. Non-kin connected and disconnected plants had greater LAR and SLA than kin connected and disconnected plants under low- and high-nutrient treatments. Plants always grew better in the presence of their kin than non-kin. These results conclude that quinoa plant production benefits from planting closely related individuals under both high- and low-nutrient conditions.

Leaf chemistry of architecturally defended plants responds more strongly to soil phosphorus variation than non-architecturally defended ones.

Plants utilize a mixture of defence types in response to herbivores, including physical, chemical, and biological defences. Among chemical defences, phenolics are well-known to inhibit digestion and are highly variable across plant species and resource gradients. There are prominent hypotheses predicting the potential change of phenolics in response to soil nutrients, but most focus on nitrogen (N) and none consider their interaction with defence strategies. We proposed an updated theoretical model that incorporates defence types and predicts their relative advantages under herbivore attack. We studied intraspecific leaf chemistry of several architecturally defended and non-architecturally defended species growing together across four sites with varying soil chemistry. We measured individual-level leaf concentrations of carbon, nitrogen, phosphorus (P), potassium (K), and phenolics, and site-level soil N, P, and K. We found that architectural defenders had lower phenolics and higher P than non-architectural defenders across locations. Relationships between soil nutrients and leaf chemistry were steeper in architectural defenders. Most leaf nutrients and phenolics showed significant relationships with soil P, and only leaf P was related to its respective soil resource. Within leaves, phenolics were negatively related to leaf N in both groups but only negatively related to leaf P for architectural defenders. Our results suggest that architectural defenders are less able to accumulate phenolic defences in high P soils than non-architectural defender. One possible explanation is that phenolic production is limited in P-rich soils via active phloem loading, but only in architectural defenders that have defence options other than chemical ones.

Fauna access outweighs litter mixture effect during leaf litter decomposition.

Decomposition rates of litter mixtures reflect the combined effects of litter species diversity, litter quality, decomposers, their interactions with each other and with the environment. The outcomes of those interactions remain ambiguous and past studies have reported conflicting results (e.g., litter mixture richness effects). To date, how litter diversity and soil fauna interactions shape litter mixture decomposition remains poorly understood. Through a sixteen month long common garden litter decomposition experiment, we tested these interaction effects using litterbags of three mesh sizes (micromesh, mesomesh, and macromesh) to disentangle the contributions of different fauna groups categorized by their size at Wuhan botanical garden (subtropical climate). We examined the decomposition of five single commonly available species litters and their full 26 mixtures combination spanning from 2 to 5 species. In total, 2325 litterbags were incubated at the setup of the experiment and partly harvested after 1, 3, 6, 9, and 16 months after exposure to evaluate the mass loss and the combined effects of soil fauna and litter diversity. We predicted that litter mixture effects should increase with increased litter quality dissimilarity, and soil fauna should enhance litter (both single species litter and litter mixtures) decomposition rate. Litter mass loss ranged from 26.9 % to 87.3 %. Soil fauna access to litterbags accelerated mass loss by 29.8 % on average. The contribution of soil mesofauna did not differ from that of soil meso- and macrofauna. Incubation duration and its interactions with litter quality dissimilarities together with soil fauna determined the litter mixture effect. Furthermore, the litter mixture effect weakened as the decomposition progresses. Faunal contribution was broadly additive to the positive mixture effect irrespective of litter species richness or litter dissimilarity. This implies that combining the dissimilarity of mixture species and contributions of different soil fauna provides a more comprehensive understanding of mixed litter decomposition.

Defence plasticity in the spiny plant Aralia elata (Miq.) Seem. in response to light and soil fertility.

BACKGROUND AND AIMS: Plants have evolved various defences against herbivores, including direct chemical and structural defences and co-opted biological defences by predatory insects. However, the effects of abiotic habitat conditions on the quantitative expression of defence traits of spiny species have not been elucidated. METHODS: Here, we investigated whether a spiny deciduous tree, Aralia elata (Miq.) Seem., changes its defence expression across light and nutrient gradients. We measured allocation to spines and C-based secondary metabolites (condensed tannins and total phenols) on A. elata plants growing across light and nutrient gradients in situ in natural landscapes in Japan. Second, we examined the effects of light and soil nutrient condition on allocation to shoot organs, spines and chemical defences of juveniles of two genotypes of the species, respectively spiny (mainland population) and non-spiny (island population), grown in a glasshouse. KEY RESULTS: In the field investigation, absolute spine mass, spine mass fraction, total phenols and condensed tannins all responded positively to canopy openness. Total phenol content was also negatively related to soil N. In the glasshouse, spiny genotype individuals had less total biomass, had lower stem allocation and were shorter than non-spiny genotype individuals. In spiny genotype trees, both spine mass fraction and total phenols decreased under low light conditions. Nutrient additions had negative effects on spine mass fraction and total phenols, but no effect on absolute spine mass. CONCLUSIONS: These results suggest that development of spines is costly for A. elata and receives greater allocation when carbohydrate supply is more plentiful. Thus, light is a more important determinant of spine allocation than soil nutrients for A. elata.

Description of two new species of Hemiphyllodactylus (Reptilia: Gekkonidae) from karst landscapes in Yunnan, China, highlights complex conservation needs.

Karst habitats are hotspots of diversity and endemism. Their naturally fragmented distributions across broad geographic landscapes have led to the complex array of smaller evolutionary ecosystems that present unique challenges from a conservation perspective. Comprehensive biodiversity assessments of karst habitats have revealed that these ecosystems contain an almost unparalleled level of endemism, and many site-restricted species remain undescribed, thus posing considerable challenges for effective conservation management. Small rock-dwelling species, such as geckos, may be particularly prone to such isolation. In this paper, we discuss one such genus, i.e., Hemiphyllodactylus, and explore its diversity across karst landforms in Yunnan Province, southwestern China. Based on morphological and genetic data, we describe two new species of Hemiphyllodactylus from karst habitats in Simao District and Yanshan County. A phylogenetic tree for Hemiphyllodactylus was constructed using 1 039 base pairs (bp) of the mitochondrial NADH dehydrogenase subunit 2 gene ( ND2). The Simao and Yanshan specimens can be distinguished from all other congeners within their respective subclades based on uncorrected genetic pairwise distances greater than 6.3% and 4.3% respectively, as well as significant morphological differences. The discovery and description of these two new species brings the total number of described Hemiphyllodactylus species in China to 14 and indicates many more undescribed species from unsurveyed karst regions await discovery. Our findings suggest that karst ecosystems in Yunnan support a higher diversity of Hemiphyllodactylus than previously known. This study also highlights the importance of karst ecosystems as refugia for site-specific endemic species and the need for heightened conservation efforts.

Rapid Eocene diversification of spiny plants in subtropical woodlands of central Tibet.

Spinescence is an important functional trait possessed by many plant species for physical defence against mammalian herbivores. The development of spinescence must have been closely associated with both biotic and abiotic factors in the geological past, but knowledge of spinescence evolution suffers from a dearth of fossil records, with most studies focusing on spatial patterns and spinescence-herbivore interactions in modern ecosystems. Numerous well-preserved Eocene (~39 Ma) plant fossils exhibiting seven different spine morphologies discovered recently in the central Tibetan Plateau, combined with molecular phylogenetic character reconstruction, point not only to the presence of a diversity of spiny plants in Eocene central Tibet but a rapid diversification of spiny plants in Eurasia around that time. These spiny plants occupied an open woodland landscape, indicated by numerous megafossils and grass phytoliths found in the same deposits, as well as numerical climate and vegetation modelling. Our study shows that regional aridification and expansion of herbivorous mammals may have driven the diversification of functional spinescence in central Tibetan woodlands, ~24 million years earlier than similar transformations in Africa.

Leaf trait association in relation to herbivore defense, drought resistance, and economics in a tropical invasive plant.

PREMISE: Exploring how functional traits vary and covary is important to understand plant responses to environmental change. However, we have limited understanding of the ways multiple functional traits vary and covary within invasive species. METHODS: We measured 12 leaf traits of an invasive plant Chromolaena odorata, associated with plant or leaf economics, herbivore defense, and drought resistance on 10 introduced populations from Asia and 12 native populations from South and Central America, selected across a broad range of climatic conditions, and grown in a common garden. RESULTS: Species' range and climatic conditions influenced leaf traits, but trait variation across climate space differed between the introduced and native ranges. Traits that confer defense against herbivores and drought resistance were associated with economic strategy, but the patterns differed by range. Plants from introduced populations that were at the fast-return end of the spectrum (high photosynthetic capacity) had high physical defense traits (high trichome density), whereas plants from native populations that were at the fast-return end of the spectrum had high drought escape traits (early leaf senescence and high percentage of withered shoots). CONCLUSIONS: Our results indicate that invasive plants can rapidly adapt to novel environmental conditions. Chromolaena odorata showed multiple different functional trait covariation patterns and clines in the native and introduced ranges. Our results emphasize that interaction between multiple traits or functions should be considered when investigating the adaptive evolution of invasive plants.

Trunk spines of trees: a physical defence against bark removal and climbing by mammals?

BACKGROUND AND AIMS: The defensive role of spines has previously been related to leaves, young shoots and reproductive organs. However, some woody species harbour spines on their trunks where none of those organs are present. Several explanations are plausible: they could be (1) climbing aids, (2) remnants from defence of leaves or reproductive organs during an earlier development phase, or (3) an as-yet undescribed defence. Here we investigate whether they could play a role against either bark feeding or preventing climbing animals accessing food resources in the tree canopy. METHODS: We described 31 woody species with spines on their trunk, growing in a botanical garden, to test whether morphological strategies could be identified and suggest what could be their most likely function. As testing their function is difficult experimentally for large pools of species, we performed virtual experiments to evaluate the potential roles of trunk spines against bark removal and climbing animals of different sizes. We then compared for each species and their confamilial non-spiny species the nutritional profiles of leaf, bark and reproductive organs to test whether trunk spines were associated with a nutritious organ (more likely targeted by herbivores). KEY RESULTS: We identified four morphological syndromes of trunk spines. Two corresponded to already known functions (anchorage for lianas and crown defence against large ground mammals), and two strategies are newly described trait syndromes with traits suggesting a defence against bark feeding and climbing mammals. By simulation, we show how each strategy could translate into defence against debarking and prevent herbivores from climbing. CONCLUSIONS: We identified trunk spine strategies and the criteria to classify them, their most likely function and the likely feeding mode and size of animal against which different trunk spine strategies may be effective. We discuss further perspectives for testing their function and their ecological significance.

Hydraulic prediction of drought-induced plant dieback and top-kill depends on leaf habit and growth form.

Hydraulic failure caused by severe drought contributes to aboveground dieback and whole-plant death. The extent to which dieback or whole-plant death can be predicted by plant hydraulic traits has rarely been tested among species with different leaf habits and/or growth forms. We investigated 19 hydraulic traits in 40 woody species in a tropical savanna and their potential correlations with drought response during an extreme drought event during the El Niño-Southern Oscillation in 2015. Plant hydraulic trait variation was partitioned substantially by leaf habit but not growth form along a trade-off axis between traits that support drought tolerance versus avoidance. Semi-deciduous species and shrubs had the highest branch dieback and top-kill (complete aboveground death) among the leaf habits or growth forms. Dieback and top-kill were well explained by combining hydraulic traits with leaf habit and growth form, suggesting integrating life history traits with hydraulic traits will yield better predictions.

A nuclear phylogenomic study of the angiosperm order Myrtales, exploring the potential and limitations of the universal Angiosperms353 probe set.

PREMISE: To further advance the understanding of the species-rich, economically and ecologically important angiosperm order Myrtales in the rosid clade, comprising nine families, approximately 400 genera and almost 14,000 species occurring on all continents (except Antarctica), we tested the Angiosperms353 probe kit. METHODS: We combined high-throughput sequencing and target enrichment with the Angiosperms353 probe kit to evaluate a sample of 485 species across 305 genera (76% of all genera in the order). RESULTS: Results provide the most comprehensive phylogenetic hypothesis for the order to date. Relationships at all ranks, such as the relationship of the early-diverging families, often reflect previous studies, but gene conflict is evident, and relationships previously found to be uncertain often remain so. Technical considerations for processing HTS data are also discussed. CONCLUSIONS: High-throughput sequencing and the Angiosperms353 probe kit are powerful tools for phylogenomic analysis, but better understanding of the genetic data available is required to identify genes and gene trees that account for likely incomplete lineage sorting and/or hybridization events.

Evolving the structure: climatic and developmental constraints on the evolution of plant architecture. A case study in Euphorbia.

Plant architecture strongly influences ecological performance, yet its role in plant evolution has not been explored in depth. By testing both phylogenetic and environmental signals, it is possible to separate architectural traits into four categories: development constraints (phylogenetic signal only); convergences (environmental dependency only); key confluences to the environmental driver (both); unknown (neither). We analysed the evolutionary history of the genus Euphorbia, a model clade with both high architectural diversity and a wide environmental range. We conducted comparative analyses of 193 Euphorbia species world-wide using 73 architectural traits, a dated phylogeny, and climate data. We identified 14 architectural types in Euphorbia based on trait combinations. We found 22 traits and three types representing convergences under climate groups, 21 traits and four types showing phylogenetic signal but no relation to climate, and 16 traits and five types with both climate and phylogenetic signals. Major drivers of architectural trait evolution likely include water stress in deserts (selected for succulence, continuous branching), frost disturbance in temperate systems (selected for simple, prostrate, short-lived shoots) and light competition (selected for arborescence). Simple architectures allowed resilience to disturbance, and frequent transitions into new forms. Complex architectures with functional specialisation developed under stable climates but have low evolvability.

Climate change promotes transitions to tall evergreen vegetation in tropical Asia.

Vegetation in tropical Asia is highly diverse due to large environmental gradients and heterogeneity of landscapes. This biodiversity is threatened by intense land use and climate change. However, despite the rich biodiversity and the dense human population, tropical Asia is often underrepresented in global biodiversity assessments. Understanding how climate change influences the remaining areas of natural vegetation is therefore highly important for conservation planning. Here, we used the adaptive Dynamic Global Vegetation Model version 2 (aDGVM2) to simulate impacts of climate change and elevated CO2 on vegetation formations in tropical Asia for an ensemble of climate change scenarios. We used climate forcing from five different climate models for representative concentration pathways RCP4.5 and RCP8.5. We found that vegetation in tropical Asia will remain a carbon sink until 2099, and that vegetation biomass increases of up to 28% by 2099 are associated with transitions from small to tall woody vegetation and from deciduous to evergreen vegetation. Patterns of phenology were less responsive to climate change and elevated CO2 than biomes and biomass, indicating that the selection of variables and methods used to detect vegetation changes is crucial. Model simulations revealed substantial variation within the ensemble, both in biomass increases and in distributions of different biome types. Our results have important implications for management policy, because they suggest that large ensembles of climate models and scenarios are required to assess a wide range of potential future trajectories of vegetation change and to develop robust management plans. Furthermore, our results highlight open ecosystems with low tree cover as most threatened by climate change, indicating potential conflicts of interest between biodiversity conservation in open ecosystems and active afforestation to enhance carbon sequestration.

Strong intraspecific trait variation in a tropical dominant tree species along an elevational gradient.

Functional trait variation of plant species includes both inter- and intraspecific variation; however, trait-based plant ecology generally considers only interspecific variation while ignoring intraspecific variation. One reason for this neglect is that intraspecific variation may be negligible when compared to interspecific variation; however, direct comparisons between inter- and intraspecific variation of plant species are lacking, especially in tropical forests. Here we investigated intraspecific leaf trait variation (leaf area, specific leaf area, leaf thickness, leaf density, leaf chlorophyll content) of Pittosporopsis kerrii Craib (Icacinaceae), the most abundant tree species in the Xishuangbanna tropical seasonal rainforest in southwestern China, along an elevational gradient (703-824 m). We found a substantial range of intraspecific variation in P. kerrii that was never less than 22.1% of range of the interspecific variation among 462 tree species reported before in the same community. Moreover, with increased elevation, both leaf thickness and density increased and specific leaf area decreased significantly. It could be more important for the individuals of P. kerrii to produce thicker and denser leaves to tolerate environmental stress (e.g. soil water availability) rather than having high growth rates at the places with higher elevation in the Xishuangbanna tropical seasonal rainforest.

Climate Change and Edaphic Specialists: Irresistible Force Meets Immovable Object?

Species exposed to anthropogenic climate change can acclimate, adapt, move, or be extirpated. It is often assumed that movement will be the dominant response, with populations tracking their climate envelopes in space, but the numerous species restricted to specialized substrates cannot easily move. In warmer regions of the world, such edaphic specialists appear to have accumulated in situ over millions of years, persisting despite climate change by local movements, plastic responses, and genetic adaptation. However, past climates were usually cooler than today and rates of warming slower, while edaphic islands are now exposed to multiple additional threats, including mining. Modeling studies that ignore edaphic constraints on climate change responses may therefore give misleading results for a significant proportion of all taxa.

Developmental constraints and resource environment shape early emergence and investment in spines in saplings.

BACKGROUND AND AIMS: Herbivory by large mammals imposes a critical recruitment bottleneck on plants in many systems. Spines defend plants against large herbivores, and how early they emerge in saplings may be one of the strongest predictors of sapling survival in herbivore-rich environments. Yet little effort has been directed at understanding the variability in spine emergence across saplings. METHODS: We present a multispecies study examining whether and how sapling size, spine type and species' environmental niche (light and precipitation environment) influence early emergence and biomass investment in spines. A phylogenetically diverse pool of 45 species possessing different spine types (spines, prickles and thorns; that are derived from distinct plant organs: leaf, epidermis or cortex, and branch, respectively), were grown under common-garden conditions, and patterns of spine emergence and biomass allocation to spines at 5 and 15 weeks after transplanting were characterized. KEY RESULTS: Spine type and species' resource niche were the main factors driving early emergence and investment patterns. Spines emerged earliest in leaf spine-bearing species, and latest in thorn-bearing species. The probability of early spine emergence increased with decreasing precipitation, and was greater in species from open than from closed habitats. Sapling investment in spines changed with plant mass but was contingent on spine type and habitat type. CONCLUSIONS: Different spine types have strikingly different timing of expression, suggesting that developmental origins of spines play a critical role in sapling defences. Furthermore, species from different precipitation and light environments (open vs. closed habitats) showed contrasting patterns of early spine expression, suggesting that resource limitation in their native range may have driven divergent evolution of early defence expression.

Tropical forest conversion to rubber plantation in southwest China results in lower fungal beta diversity and reduced network complexity.

Despite the extensive, ongoing conversion of tropical forests to rubber plantation, the effects of this land-use change on soil fungal community diversity and composition are still poorly known. We compared a network of sites of tropical forest in southern Yunnan, China, with a network of rubber plantation sites originally derived from this forest. Soil DNA was amplified for ITS2 and sequenced using Illumina MiSeq. We found that there was a major shift in community composition across all phyla, including a large reduction in ectomycorrhizal fungi likely related to the absence of hosts. Conversion from forest to rubber plantation had no effect on total fungal α-diversity, but rubber plantation had lower ß-diversity, resulting in lower overall gamma diversity. Networks based on co-occurrence of operational taxonomic unit in each land-use type showed that network complexity decreased with land-use change from forest to rubber plantation. Further investigation of soil functionality is needed to investigate whether this lower network complexity is related to reduced soil ecosystem resilience.