Plant canopies promote climatic disequilibrium in Mediterranean recruit communities.

Current rates of climate change are exceeding the capacity of many plant species to track climate, thus leading communities to be in disequilibrium with climatic conditions. Plant canopies can contribute to this disequilibrium by buffering macro-climatic conditions and sheltering poorly adapted species to the oncoming climate, particularly in their recruitment stages. Here we analyse differences in climatic disequilibrium between understorey and open ground woody plant recruits in 28 localities, covering more than 100,000 m2 , across an elevation range embedding temperature and aridity gradients in the southern Iberian Peninsula. This study demonstrates higher climatic disequilibrium under canopies compared with open ground, supporting that plant canopies would affect future community climatic lags by allowing the recruitment of less arid-adapted species in warm and dry conditions, but also it endorse that canopies could favour warm-adapted species in extremely cold environments as mountain tops, thus pre-adapting communities living in these habitats to climate change.

Phylogenetic congruence between Neotropical primates and plants is driven by frugivory.

Seed dispersal benefits plants and frugivores, and potentially drives co-evolution, with consequences to diversification evidenced for, e.g., primates. Evidence for macro-coevolutionary patterns in multi-specific, plant-animal mutualisms is scarce, and the mechanisms driving them remain unexplored. We tested for phylogenetic congruences in primate-plant interactions and showed strong co-phylogenetic signals across Neotropical forests, suggesting that both primates and plants share evolutionary history. Phylogenetic congruence between Platyrrhini and Angiosperms was driven by the most generalist primates, modulated by their functional traits, interacting with a wide-range of Angiosperms. Consistently similar eco-evolutionary dynamics seem to be operating irrespective of local assemblages, since co-phylogenetic signal emerged independently across three Neotropical regions. Our analysis supports the idea that macroevolutionary, coevolved patterns among interacting mutualistic partners are driven by super-generalist taxa. Trait convergence among multiple partners within multi-specific assemblages appears as a mechanism favouring these likely coevolved outcomes.

Net plant interactions are highly variable and weakly dependent on climate at the global scale.

Although plant-plant interactions (i.e. competition and facilitation) have long been recognised as key drivers of plant community composition and dynamics, their global patterns and relationships with climate have remained unclear. Here, we assembled a global database of 10,502 pairs of empirical data from the literature to address the patterns of and climatic effects on the net outcome of plant interactions in natural communities. We found that plant interactions varied among plant performance indicators, interaction types and biomes, yet competition occurred more frequently than facilitation in plant communities worldwide. Unexpectedly, plant interactions showed weak latitudinal pattern and were weakly related to climate. Our study provides a global comprehensive overview of plant interactions, highlighting competition as a fundamental mechanism structuring plant communities worldwide. We suggest that further investigations should focus more on local factors (e.g. microclimate, soil and disturbance) than on macroclimate to identify key environmental determinants of interactions in plant communities.

The phylogenetic roots of human lethal violence.

The psychological, sociological and evolutionary roots of conspecific violence in humans are still debated, despite attracting the attention of intellectuals for over two millennia. Here we propose a conceptual approach towards understanding these roots based on the assumption that aggression in mammals, including humans, has a significant phylogenetic component. By compiling sources of mortality from a comprehensive sample of mammals, we assessed the percentage of deaths due to conspecifics and, using phylogenetic comparative tools, predicted this value for humans. The proportion of human deaths phylogenetically predicted to be caused by interpersonal violence stood at 2%. This value was similar to the one phylogenetically inferred for the evolutionary ancestor of primates and apes, indicating that a certain level of lethal violence arises owing to our position within the phylogeny of mammals. It was also similar to the percentage seen in prehistoric bands and tribes, indicating that we were as lethally violent then as common mammalian evolutionary history would predict. However, the level of lethal violence has changed through human history and can be associated with changes in the socio-political organization of human populations. Our study provides a detailed phylogenetic and historical context against which to compare levels of lethal violence observed throughout our history.

Phenotypic structure of plant facilitation networks.

Identifying the plant traits that determine the outcome of facilitation interactions is essential to understand how communities are assembled and can be restored. Plant facilitation networks are phylogenetically structured but which traits are behind such a pattern is unknown. We sampled plant interactions in stressful ecosystems from south-eastern Spain to build seedling and adult facilitation networks. We collected 20 morphological and ecophysiological traits for 151 species involved in interactions between 879 nurse individuals benefiting 24 584 seedlings and adults. We detected a significant phenotypic signal in the seedling facilitation network that was maintained in the adult network, whereby functionally similar nurses tended to facilitate functionally similar species whose traits differ from those of their nurses. We provide empirical evidence to support a long-lasting theoretical postulate stating that facilitation networks are phenotypically structured. Trait matching through which nurse and facilitated species avoid phenotypic overlap, and consequently competition, is the main linkage rule shaping plant facilitation networks.

nir gene-based co-occurrence patterns reveal assembly mechanisms of soil denitrifiers in response to fire.

Denitrification causes nitrogen losses from terrestrial ecosystems. The magnitude of nitrogen loss depends on the prevalence of denitrifiers, which show ecological differences if they harbour nirS or nirK genes encoding nitrite reductases with the same biological function. Thus, it is relevant to understand the mechanisms of co-existence of denitrifiers, including their response to environmental filters and competition due to niche similarities. We propose a framework to analyse the co-existence of denitrifiers across multiple assemblages by using nir gene-based co-occurrence networks. We applied it in Mediterranean soils before and during 1 year after an experimental fire. Burning did not modify nir community structure, but significantly impacted co-occurrence patterns. Bacteria with the same nir co-occurred in space, and those with different nir excluded each other, reflecting niche requirements: nirS abundance responded to nitrate and salinity, whereas nirK to iron content. Prior to fire, mutual exclusion between bacteria with the same nir suggested competition due to niche similarities. Burning provoked an immediate rise in mineral nitrogen and erased the signals of competition, which emerged again within days as nir abundances peaked. nir co-occurrence patterns can help infer the assembly mechanisms of denitrifying communities, which control nitrogen losses in the face of ecological disturbance.

Killing conspecific adults in mammals.

Mammals kill both conspecific infants and adults. Whereas infanticide has been profusely studied, the killing of non-infants (adulticide) has seldom attracted the attention of researchers. Mammals kill conspecific adults by at least four, non-exclusive reasons: during intrasexual aggression for mating opportunities, to defend valuable resources, to protect their progeny and to prey upon conspecifics. In this study, we test which reason is most likely to explain male and female adulticide in mammals. For this, we recorded the presence of adulticide, the ecological and behavioural traits, and the phylogenetic relationship for more than 1000 species. Adulticide has been recorded in over 350 species from the most important Mammalian clades. Male adulticide was phylogenetically correlated with the presence of size dimorphism and intrasexually selected weapons. Female adulticide was phylogenetically associated with the occurrence of infanticide. These results indicate that the evolutionary pathways underlying the evolution of adulticide differ between sexes in mammals. Whereas males commit adulticide to increase breeding opportunities and to compete with other males for mating, females commit adulticide mainly to defend offspring from infanticidal conspecifics.

Ectomycorrhizal fungal diversity decreases in Mediterranean pine forests adapted to recurrent fires.

Fire is a major disturbance linked to the evolutionary history and climate of Mediterranean ecosystems, where the vegetation has evolved fire-adaptive traits (e.g., serotiny in pines). In Mediterranean forests, mutualistic feedbacks between trees and ectomycorrhizal (ECM) fungi, essential for ecosystem dynamics, might be shaped by recurrent fires. We tested how the structure and function of ECM fungal communities of Pinus pinaster and Pinus halepensis vary among populations subjected to high and low fire recurrence in Mediterranean ecosystems, and analysed the relative contribution of environmental (climate, soil properties) and tree-mediated (serotiny) factors. For both pines, local and regional ECM fungal diversity were lower in areas of high than low fire recurrence, although certain fungal species were favoured in the former. A general decline of ECM root-tip enzymatic activity for P. pinaster was associated with high fire recurrence, but not for P. halepensis. Fire recurrence and fire-related factors such as climate, soil properties or tree phenotype explained these results. In addition to the main influence of climate, the tree fire-adaptive trait serotiny recovered a great portion of the variation in structure and function of ECM fungal communities associated with fire recurrence. Edaphic conditions (especially pH, tightly linked to bedrock type) were an important driver shaping ECM fungal communities, but mainly at the local scale and probably independently of the fire recurrence. Our results show that ECM fungal community shifts are associated with fire recurrence in fire-prone dry Mediterranean forests, and reveal complex feedbacks among trees, mutualistic fungi and the surrounding environment in these ecosystems.

Plant facilitation through mycorrhizal symbiosis is stronger between distantly related plant species.

The tendency of closely related plant species to share natural enemies has been suggested to limit their co-occurrence and performance, but we lack a deep understanding on how mutualistic interactions such as the mycorrhizal symbiosis affect plant-plant interactions depending on the phylogenetic relatedness of the interacting plants. We hypothesise that the effect of the mycorrhizal symbiosis on plant-plant facilitative interactions depends on the phylogenetic distance between the nurse and facilitated plants. A recently published meta-analysis compiled the strength of plant facilitative interactions in the presence or absence (or reduced abundance) of mycorrhizal fungi. We use phylogenetically informed Bayesian linear models to test whether the effect size is influenced by the phylogenetic distance between the plant species involved in each plant facilitative interaction. Conspecific facilitative interactions are more strongly enhanced by mycorrhizal fungi than interactions between closely related species. In heterospecific interactions, the effect of the mycorrhizal symbiosis on plant facilitation increases with the phylogenetic distance between the nurse and facilitated plant species. Our result showing that the effect of mycorrhizal symbiosis on the facilitation interactions between plants depends on their phylogenetic relatedness provides new mechanisms to understand how facilitation is assembling ecological communities.

Successional trajectories of soil bacterial communities in mine tailings: The role of plant functional traits.

Plant species identity is assumed to be a major driver of belowground microbial diversity and composition. However, diagnosing which plant functional traits are responsible for shaping microbial communities remains elusive. Primary succession on barren metalliferous mining substrates was selected as the framework to study above-belowground interactions, and plant functional traits that lead the successional trajectories of soil bacterial communities were identified. The impact of the plant functional group (i.e. trees, shrubs, dwarf shrubs, perennial grasses), a trait integrating the life span and morphological structure, on the bacterial primary succession was monitored. Bacterial diversity and composition was estimated along plant size gradients including over 90 scattered patches ranging from seedlings to mature multispecific patches. Soil bacterial diversity was affected by heavy metals levels and increased towards higher resource availability underneath mature patches, with stress-tolerant heterotrophs and phototrophs being replaced by competitive heterotrophs. The plant functional group modulated these general patterns and shrubs had the greatest impact belowground by inducing the largest increase in soil fertility. Functional traits related to leaf decomposability and root architecture further determined the composition and structure of bacterial communities. These results underline the importance of plant functional traits in the assembly of soil bacterial communities, and can help guiding restoration of degraded lands.

Resilience to fire of phylogenetic diversity across biological domains.

Fire alters the structure and composition of above- and belowground communities with concurrent shifts in phylogenetic diversity. The inspection of postfire trends in the diversity of ecological communities incorporating phylogenetic information allows to better understand the mechanisms driving fire resilience. While fire reduces plant phylogenetic diversity based on the recruitment of evolutionarily related species with postfire seed persistence, it increases that of soil microbes by limiting soil resources and changing the dominance of competing microbes. Thus, during postfire community reassembly, plant and soil microbes might experience opposing temporal trends in their phylogenetic diversity that are linked through changes in the soil conditions. We tested this hypothesis by investigating the postfire evolution of plant and soil microbial (fungi, bacteria and archaea) communities across three 20-year chronosequences. Plant phylogenetic diversity increased with time since fire as pioneer seeders facilitate the establishment of distantly related late-successional shrubs. The postfire increase in plant phylogenetic diversity fostered plant productivity, eventually recovering soil organic matter. These shifts over time in the soil conditions explained the postfire restoration of fungal and bacterial phylogenetic diversity, which decreased to prefire levels, suggesting that evolutionarily related taxa with high relative fitness recover their competitive superiority during community reassembly. The resilience to fire of phylogenetic diversity across biological domains helps preserve the evolutionary history stored in our ecosystems.

Fire modifies the phylogenetic structure of soil bacterial co-occurrence networks.

Fire alters ecosystems by changing the composition and community structure of soil microbes. The phylogenetic structure of a community provides clues about its main assembling mechanisms. While environmental filtering tends to reduce the community phylogenetic diversity by selecting for functionally (and hence phylogenetically) similar species, processes like competitive exclusion by limiting similarity tend to increase it by preventing the coexistence of functionally (and phylogenetically) similar species. We used co-occurrence networks to detect co-presence (bacteria that co-occur) or exclusion (bacteria that do not co-occur) links indicative of the ecological interactions structuring the community. We propose that inspecting the phylogenetic structure of co-presence or exclusion links allows to detect the main processes simultaneously assembling the community. We monitored a soil bacterial community after an experimental fire and found that fire altered its composition, richness and phylogenetic diversity. Both co-presence and exclusion links were more phylogenetically related than expected by chance. We interpret such a phylogenetic clustering in co-presence links as a result of environmental filtering, while that in exclusion links reflects competitive exclusion by limiting similarity. This suggests that environmental filtering and limiting similarity operate simultaneously to assemble soil bacterial communities, widening the traditional view that only environmental filtering structures bacterial communities.

Nurse plants transfer more nitrogen to distantly related species.

Plant facilitative interactions enhance co-occurrence between distant relatives, partly due to limited overlap in resource requirements. We propose a different mechanism for the coexistence of distant relatives based on positive interactions of nutrient sharing. Nutrients move between plants following source-sink gradients driven by plant traits that allow these gradients to establish. Specifically, nitrogen (N) concentration gradients can arise from variation in leaf N content across plants species. As many ecologically relevant traits, we hypothesize that leaf N content is phylogenetically conserved and can result in N gradients promoting N transfer among distant relatives. In a Mexican desert community governed by facilitation, we labelled nurse plants (Mimosa luisana) with 15 N and measured its transfer to 14 other species in the community, spanning the range of phylogenetic distances to the nurse plant. Nurses established steeper N source-sink gradients with distant relatives, increasing 15 N transfer toward these species. Nutrient sharing may provide long-term benefits to facilitated plants and may be an overlooked mechanism maintaining coexistence and increasing the phylogenetic diversity of plant communities.

Increased fire frequency promotes stronger spatial genetic structure and natural selection at regional and local scales in Pinus halepensis Mill.

Background and Aims: The recurrence of wildfires is predicted to increase due to global climate change, resulting in severe impacts on biodiversity and ecosystem functioning. Recurrent fires can drive plant adaptation and reduce genetic diversity; however, the underlying population genetic processes have not been studied in detail. In this study, the neutral and adaptive evolutionary effects of contrasting fire regimes were examined in the keystone tree species Pinus halepensis Mill. (Aleppo pine), a fire-adapted conifer. The genetic diversity, demographic history and spatial genetic structure were assessed at local (within-population) and regional scales for populations exposed to different crown fire frequencies. Methods: Eight natural P. halepensis stands were sampled in the east of the Iberian Peninsula, five of them in a region exposed to frequent crown fires (HiFi) and three of them in an adjacent region with a low frequency of crown fires (LoFi). Samples were genotyped at nine neutral simple sequence repeats (SSRs) and at 251 single nucleotide polymorphisms (SNPs) from coding regions, some of them potentially important for fire adaptation. Key Results: Fire regime had no effects on genetic diversity or demographic history. Three high-differentiation outlier SNPs were identified between HiFi and LoFi stands, suggesting fire-related selection at the regional scale. At the local scale, fine-scale spatial genetic structure (SGS) was overall weak as expected for a wind-pollinated and wind-dispersed tree species. HiFi stands displayed a stronger SGS than LoFi stands at SNPs, which probably reflected the simultaneous post-fire recruitment of co-dispersed related seeds. SNPs with exceptionally strong SGS, a proxy for microenvironmental selection, were only reliably identified under the HiFi regime. Conclusions: An increasing fire frequency as predicted due to global change can promote increased SGS with stronger family structures and alter natural selection in P. halepensis and in plants with similar life history traits.

The phylogenetic structure of plant-pollinator networks increases with habitat size and isolation.

Similarity among species in traits related to ecological interactions is frequently associated with common ancestry. Thus, closely related species usually interact with ecologically similar partners, which can be reinforced by diverse co-evolutionary processes. The effect of habitat fragmentation on the phylogenetic signal in interspecific interactions and correspondence between plant and animal phylogenies is, however, unknown. Here, we address to what extent phylogenetic signal and co-phylogenetic congruence of plant-animal interactions depend on habitat size and isolation by analysing the phylogenetic structure of 12 pollination webs from isolated Pampean hills. Phylogenetic signal in interspecific interactions differed among webs, being stronger for flower-visiting insects than plants. Phylogenetic signal and overall co-phylogenetic congruence increased independently with hill size and isolation. We propose that habitat fragmentation would erode the phylogenetic structure of interaction webs. A decrease in phylogenetic signal and co-phylogenetic correspondence in plant-pollinator interactions could be associated with less reliable mutualism and erratic co-evolutionary change.

Opposing phylogenetic diversity gradients of plant and soil bacterial communities.

Plants and soil microbes show parallel patterns of species-level diversity. Diverse plant communities release a wider range of organics that are consumed by more microbial species. We speculated, however, that diversity metrics accounting for the evolutionary distance across community members would reveal opposing patterns between plant and soil bacterial phylogenetic diversity. Plant phylogenetic diversity enhances plant productivity and thus expectedly soil fertility. This, in turn, might reduce bacterial phylogenetic diversity by favouring one (or a few) competitive bacterial clade. We collected topsoils in 15 semi-arid plant patches and adjacent low-cover areas configuring a plant phylodiversity gradient, pyrosequenced the 16S rRNA gene to identify bacterial taxa and analysed soil fertility parameters. Structural equation modelling showed positive effects of both plant richness and phylogenetic diversity on soil fertility. Fertility increased bacterial richness but reduced bacterial phylogenetic diversity. This might be attributed to the competitive dominance of a lineage based on its high relative fitness. This suggests biotic interactions as determinants of the soil bacterial community assembly, while emphasizing the need to use phylogeny-informed metrics to tease apart the processes underlying the patterns of diversity.

Ecological interactions are evolutionarily conserved across the entire tree of life.

Ecological interactions are crucial to understanding both the ecology and the evolution of organisms. Because the phenotypic traits regulating species interactions are largely a legacy of their ancestors, it is widely assumed that ecological interactions are phylogenetically conserved, with closely related species interacting with similar partners. However, the existing empirical evidence is inadequate to appropriately evaluate the hypothesis of phylogenetic conservatism in ecological interactions, because it is both ecologically and taxonomically biased. In fact, most studies on the evolution of ecological interactions have focused on specialized organisms, such as some parasites or insect herbivores, belonging to a limited subset of the overall tree of life. Here we study the evolution of host use in a large and diverse group of interactions comprising both specialist and generalist acellular, unicellular and multicellular organisms. We show that, as previously found for specialized interactions, generalized interactions can be evolutionarily conserved. Significant phylogenetic conservatism of interaction patterns was equally likely to occur in symbiotic and non-symbiotic interactions, as well as in mutualistic and antagonistic interactions. Host-use differentiation among species was higher in phylogenetically conserved clades, irrespective of their generalization degree and taxonomic position within the tree of life. Our findings strongly suggest a shared pattern in the organization of biological systems through evolutionary time, mediated by marked conservatism of ecological interactions among taxa.

Centrality in primate-parasite networks reveals the potential for the transmission of emerging infectious diseases to humans.

Most emerging infectious diseases (EIDs) in humans have arisen from animals. Identifying high-risk hosts is therefore vital for the control and surveillance of these diseases. Viewing hosts as connected through the parasites they share, we use network tools to investigate predictors of parasitism and sources of future EIDs. We generated host-parasite networks that link hosts when they share a parasite, using nonhuman primates as a model system because--owing to their phylogenetic proximity and ecological overlap with humans--they are an important source of EIDs to humans. We then tested whether centrality in the network of host species--a measurement of the importance of a given node (i.e., host species) in the network--is associated with that host serving as a potential EID source. We found that centrality covaries with key predictors of parasitism, such as population density and geographic range size. Importantly, we also found that primate species having higher values of centrality in the primate-parasite network harbored more parasites identified as EIDs in humans and had parasite communities more similar to those found in humans. These relationships were robust to the use of different centrality metrics and to multiple ways of controlling for variation in how well each species has been studied (i.e., sampling effort). Centrality may therefore estimate the role of a host as a source of EIDs to humans in other multispecific host-parasite networks.

Abiotic stress tolerance and competition-related traits underlie phylogenetic clustering in soil bacterial communities.

Soil bacteria typically coexist with close relatives generating widespread phylogenetic clustering. This has been ascribed to the abiotic filtering of organisms with shared ecological tolerances. Recent theoretical developments suggest that competition can also explain the phylogenetic similarity of coexisting organisms by excluding large low-competitive clades. We propose that combining the environmental patterns of traits associated with abiotic stress tolerances or competitive abilities with phylogeny and abundance data, can help discern between abiotic and biotic mechanisms underlying the coexistence of phylogenetically related bacteria. We applied this framework in a model system composed of interspersed habitats of highly contrasted productivity and comparatively dominated by biotic and abiotic processes, i.e. the plant patch-gap mosaic typical of drylands. We examined the distribution of 15 traits and 3290 bacterial taxa in 28 plots. Communities showed a marked functional response to the environment. Conserved traits related to environmental stress tolerance (e.g. desiccation, formation of resistant structures) were differentially selected in either habitat, while competition related traits (e.g. organic C consumption, formation of nutrient-scavenging structures) prevailed under high resource availability. Phylogenetic clustering was stronger in habitats dominated by biotic filtering, suggesting that competitive exclusion of large clades might underlie the ecological similarity of co-occurring soil bacteria.

In situ genetic association for serotiny, a fire-related trait, in Mediterranean maritime pine (Pinus pinaster).

Wildfire is a major ecological driver of plant evolution. Understanding the genetic basis of plant adaptation to wildfire is crucial, because impending climate change will involve fire regime changes worldwide. We studied the molecular genetic basis of serotiny, a fire-related trait, in Mediterranean maritime pine using association genetics. A single nucleotide polymorphism (SNP) set was used to identify genotype : phenotype associations in situ in an unstructured natural population of maritime pine (eastern Iberian Peninsula) under a mixed-effects model framework. RR-BLUP was used to build predictive models for serotiny in this region. Model prediction power outside the focal region was tested using independent range-wide serotiny data. Seventeen SNPs were potentially associated with serotiny, explaining approximately 29% of the trait phenotypic variation in the eastern Iberian Peninsula. Similar prediction power was found for nearby geographical regions from the same maternal lineage, but not for other genetic lineages. Association genetics for ecologically relevant traits evaluated in situ is an attractive approach for forest trees provided that traits are under strong genetic control and populations are unstructured, with large phenotypic variability. This will help to extend the research focus to ecological keystone non-model species in their natural environments, where polymorphisms acquired their adaptive value.