The Hierarchical Coevolutionary Units of Ecological Networks.

In ecological networks, cohesive groups of species may shape the evolution of interactions, serving as coevolutionary units. Ranging across network scales, from motifs to isolated components, elucidating which cohesive groups are more determinant for coevolution remains a challenge in ecology. We address this challenge by integrating 376 empirical mutualistic and antagonistic networks and coevolutionary models. We identified cohesive groups at four network scales containing a significant proportion of potential direct coevolutionary effects. Cohesive groups displayed hierarchical organisation, and potential coevolutionary effects overflowing lower-scale groups were contained by higher-scale groups, underscoring the hierarchy's impact. However, indirect coevolutionary effects blurred group boundaries and hierarchy, particularly under strong selection from ecological interactions. Thus, under strong selection, indirect effects render networks themselves, and not cohesive groups, as the likely coevolutionary units of ecological systems. We hypothesise hierarchical cohesive groups to also shape how other forms of direct and indirect effects propagate in ecological systems.

The coevolution of fungus-ant agriculture.

Fungus-farming ants cultivate multiple lineages of fungi for food, but, because fungal cultivar relationships are largely unresolved, the history of fungus-ant coevolution remains poorly known. We designed probes targeting >2000 gene regions to generate a dated evolutionary tree for 475 fungi and combined it with a similarly generated tree for 276 ants. We found that fungus-ant agriculture originated ~66 million years ago when the end-of-Cretaceous asteroid impact temporarily interrupted photosynthesis, causing global mass extinctions but favoring the proliferation of fungi. Subsequently, ~27 million years ago, one ancestral fungal cultivar population became domesticated, i.e., obligately mutualistic, when seasonally dry habitats expanded in South America, likely isolating the cultivar population from its free-living, wet forest-dwelling conspecifics. By revealing these and other major transitions in fungus-ant coevolution, our results clarify the historical processes that shaped a model system for nonhuman agriculture.

Do Streptomyces sp. Help Mycorrhization in Raspberry?

Actinobacteria may help the mycorrhizal symbiosis by producing various bioactive metabolites. Mycorrhizae, in turn, are very important since they increase the absorption of nutrients, promoting the growth of their host plant and making inoculation with arbuscular mycorrhizae fungi (AM) a common practice applied in agriculture and forestry. The cultivation of Rubus idaeus (raspberry) is widespread in Patagonia, Argentina; however, the potential benefits of using actinobacteria-mycorrhizal inoculums to enhance crop growth and yield remain unexplored. The objective of this work was to study the interaction between actinobacteria (Streptomyces, Actinomycetota) and AM in raspberry plants. We performed an experiment applying 4 treatments to raspberry plants growing in two substrates, sterile soil and natural (non-sterile) soil. The treatments consisted in a control (without inoculation) and three inoculations treatments (AM, Streptomyces SH9 strain, and AM + Streptomyces). After 3 months of inoculation, mycorrhization parameters (%) and plant growth were recorded. When comparing both substrates, the mycorrhization parameters were higher in natural soil than in sterile soil. The co-inoculation with AM + Streptomyces SH9 showed the highest mycorrhization. Both factors (treatment x substrate) interacted showing that in sterile soil the treatments with the highest effect on mycorrhization parameters were AM and the co-inoculation, while in natural soil all inoculations improved mycorrhization parameters, being highest with the co-inoculation. These results show that Streptomyces SH9 strain helps the mycorrhizal symbiosis in raspberry, being the first report about the effect of a native rhizospheric actinobacterium on an economically important species, promising potential for environmentally friendly improvements in raspberry crops within the temperate Southern Patagonian region.

Fire and ant interactions mediated by honeydew and extrafloral nectar in an australian tropical savanna.

Fire is a major disturbance affecting ecosystems globally, but its impact on mutualisms has received minimal attention. Here, we use a long-term field experiment to investigate the impact of different fire regimes on globally important ant-honeydew and ant-extrafloral nectar (EFN) mutualistic interactions in an Australian tropical savanna. These interactions provide ants with a key energy source, while their plant and hemipteran hosts receive protection services. We examined ant interactions on species of Eucalyptus (lacking EFNs) and Acacia (with EFNs) in three replicate plots each of burning every 2 and 3 years early in the dry season, burning late in the dry season every 2 years, and unburnt for > 25 years. The proportions of plants with ant-honeydew interactions in Acacia (44.6%) and Eucalyptus (36.3%) were double those of Acacia plants with ant-EFN interactions (18.9%). The most common ants, representing 85% of all interactions, were behaviourally dominant species of Oecophylla, Iridomyrmex and Papyrius. Fire promoted the incidence of ant interactions, especially those involving EFNs on Acacia, which occurred on only 3% of plants in unburnt plots compared with 24% in frequently burnt plots. Fire also promoted the relative incidence of behaviourally dominant ants, which are considered the highest quality mutualists. Contrary to expectations, frequent fire did not result in a switching of behaviourally dominant ant partners from forest-adapted Oecophylla to arid-adapted Iridomyrmex. Our findings that frequent fire increases ant interactions mediated by honeydew and extrafloral nectar, and promotes the quality of ant mutualists, have important implications for protective services provided by ants in highly fire-prone ecosystems.

An Aphid Pest Superclone Benefits From a Facultative Bacterial Endosymbiont in a Host-Dependent Manner, Leading to Reproductive and Proteomic Changes.

The English grain aphid, Sitobion avenae, is a significant agricultural pest affecting wheat, barley, and oats. In Chile, the most prevalent and persistent clone (superclone) of S. avenae harbors the facultative endosymbiont bacterium Regiella insecticola. To determine the role of this bacterium in the reproductive success of this superclone, the presence of R. insecticola was manipulated to assess its impact on (1) the reproductive performance of this clone on two host plant species (wheat and barley), (2) the production of winged morphs, (3) changes in the insects' proteomic profiles, and (4) the root/shoot ratio of plant. It was found that the reproductive performance of this S. avenae superclone varied across host plants, depending on the presence of the facultative bacterial endosymbiont. Aphids infected with R. insecticola showed higher reproductive success on wheat, while the opposite effect was observed on barley. Aphid biomass was greater when infected with R. insecticola, particularly on barley. Additionally, aphids harboring R. insecticola exhibited a higher proportion of winged individuals on both host plants. Protein regulation in aphids on wheat was lower compared to those on barley. A higher root/shoot biomass ratio was observed in wheat plants compared to barley when infested by R. insecticola-infected aphid. Thus, R. insecticola significantly influences the reproductive performance and proteomic profile of a S. avenae superclone, with these effects shaped by the host plant. This suggests that the interaction between the host plant and the facultative endosymbiont contributes to the ecological success of this superclone.

Putting the puzzle together: the relationship between floral characters and pollinator morphology determines pollination mode in the fig-fig wasp mutualism.

The diversification of angiosperms has largely been attributed to adaptive radiation of their pollination and mating systems, which are relevant drivers of the macroevolution processes. The fig (Ficus, Moraceae) and fig wasp (Agaonidae, Hymenoptera) interaction is an example of obligate mutualism. Passive and active pollination modes have been associated with morphological traits in both partners. However, more information is required to assess the relationship between floral traits and pollination modes, particularly in Neotropical Ficus species. This study evaluates the morphological traits of figs and fig wasps regarding pollination modes in species belonging to Neotropical Ficus sections (three species each of Americanae and Pharmacosycea). Pollination mode was identified by floral morphology, anther/ovule ratio, and specialized structures fig wasps use for pollen transport (pollen pocket and coxal combs). Fig species in sect. Americanae are actively pollinated because pistillate flowers form a synstigma, present anther/ovule ratios <0.11, and their pollinator Pegoscapus fig wasps have pollen pockets and coxal combs. In contrast, species in sect. Pharmacosycea have free pistillate flowers, with anther/ovule ratios >0.27; they are pollinated by Tetrapus wasps, which lack specialized structures to carry pollen. Each species of Ficus was associated with a single morphospecies of fig wasp. The results support previous contributions that consider reciprocal morphological traits between fig species and their pollinating wasps as evidence of a close co-evolutionary history.

First report of the association between Wolbachia and Cotesia flavipes (Hymenoptera: Braconidae): effect on life history parameters of the parasitoid.

The symbiosis between microorganisms and host arthropods can cause biological, physiological, and reproductive changes in the host population. The present study aimed to survey facultative symbionts of the genera Wolbachia, Arsenophonus, Cardinium, Rickettsia, and Nosema in Cotesia flavipes (Cameron) (Hymenoptera: Braconidae) and Diatraea saccharalis (Fabricius) (Lepidoptera: Crambidae) in the laboratory and evaluate the influence of infection on the fitness of these hosts. For this purpose, 16S rDNA primers were used to detect these facultative symbionts in the host species, and the hosts' biological and morphological features were evaluated for changes resulting from the infection caused by these microorganisms. The bacterial symbionts studied herein were not detected in the D. saccharalis samples analysed, but the endosymbiont Wolbachia was detected in C. flavipes and altered the biological and morphological aspects of this parasitoid insect. The results of this study may help to elucidate the role of Wolbachia in maintaining the quality of populations/lineages of C. flavipes.

Molecular evidence of pathogens and endosymbionts in the black horse fly Osca lata (Diptera: Tabanidae) in Southern Chile.

Little is known about the role of horse flies in potential pathogen transmission in Chile. This study provides evidence of the molecular detection of microorganisms in southern Chile. In the present study, adult Osca lata horse flies were trapped from Punucapa (39°45'06"S/73°16'08"W, Región de Los Ríos) and Puyehue (40°39'10"S/72°10'57"W, Región de Los Lagos), Chile. Among the 95 samples analyzed by PCR using specific primers, microorganisms were detected in 23.2% (n = 22) of the samples. Rickettsia spp. DNA was detected in 15.8% (n = 15) of the samples, Trypanosomatidae DNA in 5.3% (n = 5) of the samples, and filarial DNA in 2.1% (n = 2) of the samples. This study found that horse flies in the region are capable of carrying a variety of both parasites and endosymbionts. Further research is needed to understand the specific impact of horse flies as mechanical or biological vectors and develop effective control measures to prevent the spread of any microorganisms associated with disease.

Evaluating quasi-experimental approaches for estimating epidemiological efficacy of non-randomised field trials: applications in Wolbachia interventions for dengue.

BACKGROUND: Wolbachia symbiosis in Aedes aegypti is an emerging biocontrol measure against dengue. However, assessing its real-world efficacy is challenging due to the non-randomised, field-based nature of most intervention studies. This research re-evaluates the spatial-temporal impact of Wolbachia interventions on dengue incidence using a large battery of quasi-experimental methods and assesses each method's validity. METHODS: A systematic search for Wolbachia intervention data was conducted via PUBMED. Efficacy was reassessed using commonly-used quasi-experimental approaches with extensive robustness checks, including geospatial placebo tests and a simulation study. Intervention efficacies across multiple study sites were computed using high-resolution aggregations to examine heterogeneities across sites and study periods. We further designed a stochastic simulation framework to assess the methods' ability to estimate intervention efficacies (IE). RESULTS: Wolbachia interventions in Singapore, Malaysia, and Brazil significantly decreased dengue incidence, with reductions ranging from 48.17% to 69.19%. IEs varied with location and duration. Malaysia showed increasing efficacy over time, while Brazil exhibited initial success with subsequent decline, hinting at operational challenges. Singapore's strategy was highly effective despite partial saturation. Simulations identified Synthetic Control Methods (SCM) and its variant, count Synthetic Control Method (cSCM), as superior in precision, with the smallest percentage errors in efficacy estimation. These methods also demonstrated robustness in placebo tests. CONCLUSIONS: Wolbachia interventions exhibit consistent protective effects against dengue. SCM and cSCM provided the most precise and robust estimates of IEs, validated across simulated and real-world settings.

Sequencing, assembly, and genomic annotation of Leucoagaricus gongylophorus LEU18496, a dikarya mutualistic species.

The basidiomycete fungus Leucoagaricus gongylophorus is able to grow in the fungus garden of leaf-cutter ants. This mutualistic interaction has driven the evolutionary adaptation of L. gongylophorus, shaping its metabolism to produce enzymes adept at lignocellulosic biomass degradation. In this study, we undertook the comprehensive sequencing, assembly, and functional annotation of the genome of L. gongylophorus strain LEU18496, mutualistic fungus of the Atta mexicana. Our genomic analyses revealed a distinctive bimodal nature to the genome: a predominant region characterized by AT enrichment and low genetic density, alongside a smaller region exhibiting higher GC content and higher genetic density. The presence of transposable elements (TEs) within the AT-enriched region suggests genomic compartmentalization, facilitating differential evolutionary rates. With a gene count of 6748, the assembled genome of L. gongylophorus LEU18496 surpasses previous reports for this fungal species. Inspection of genes associated with central metabolism unveiled a remarkable abundance of carbohydrate-active enzymes (CAZymes) and fungal oxidative lignin enzymes (FOLymes), underscoring their pivotal roles in the life cycle of this fungus.

Heme metabolism in Strigomonas culicis: Implications of H2O2 resistance induction and symbiont elimination.

Monoxenous trypanosomatid Strigomonas culicis harbors an endosymbiotic bacterium, which enables the protozoa to survive without heme supplementation. The impact of H2O2 resistance and symbiont elimination on intracellular heme and Fe2+ availability was analyzed through a comparison of WT strain with both WT H2O2-resistant (WTR) and aposymbiotic (Apo) protozoa. The relative quantification of the heme biosynthetic pathway through label-free parallel reaction monitoring targeted mass spectrometry revealed that H2O2 resistance does not influence the abundance of tryptic peptides. However, the Apo strain showed increased coproporphyrinogen III oxidase and ferrochelatase levels. A putative ferrous iron transporter, homologous to LIT1 and TcIT from Leishmania major and Trypanosoma cruzi, was identified for the first time. Label-free parallel reaction monitoring targeted mass spectrometry also showed that S. culicis Iron Transporter (ScIT) increased 1.6- and 16.4-fold in WTR and Apo strains compared to WT. Accordingly, antibody-mediated blockage of ScIT decreased by 28.0% and 40.0% intracellular Fe2+concentration in both WTR and Apo strains, whereas no effect was detected in WT. In a heme-depleted medium, adding 10 µM hemin decreased ScIT transcript levels in Apo, whereas 10 µM PPIX, the substrate of ferrochelatase, increased intracellular Fe2+ concentration and ferric iron reduction. Overall, the data suggest mechanisms dependent on de novo heme synthesis (and its substrates) in the Apo strain to overcome reduced heme availability. Given the importance of heme and Fe2+ as cofactors in metabolic pathways, including oxidative phosphorylation and antioxidant systems, this study provides novel mechanistic insights associated with H2O2 resistance in S. culicis.

Long-term strict ant-plant mutualism identity characterises growth rate and leaf shearing resistance of an Amazonian myrmecophyte.

Over 125 million years of ant-plant interactions have culminated in one of the most intriguing evolutionary outcomes in life history. The myrmecophyte Duroia hirsuta (Rubiaceae) is known for its mutualistic association with the ant Myrmelachista schumanni and several other species, mainly Azteca, in the north-western Amazon. While both ants provide indirect defences to plants, only M. schumanni nests in plant domatia and has the unique behaviour of clearing the surroundings of its host tree from heterospecific plants, potentially increasing resource availability to its host. Using a 12-year survey, we asked how the continuous presence of either only M. schumanni or only Azteca spp. benefits the growth and defence traits of host trees. We found that the continuous presence of M. schumanni improved relative growth rates and leaf shearing resistance of Duroia better than trees with Azteca. However, leaf herbivory, dry matter content, trichome density, and secondary metabolite production were the same in all trees. Survival depended directly on ant association (> 94% of trees died when ants were absent). This study extends our understanding of the long-term effects of strict ant-plant mutualism on host plant traits in the field and reinforces the use of D. hirsuta-M. schumanni as a model system suitable for eco-co-evolutionary research on plant-animal interactions.

Comparative genomics of the carmine cochineal symbiont Candidatus Dactylopiibacterium carminicum reveals possible protection to the host against viruses via CRISPR/Cas.

We present new genomes from the bacterial symbiont Candidatus Dactylopiibacterium carminicum obtained from non-domesticated carmine cochineals belonging to the scale insect Dactylopius (Hemiptera: Coccoidea: Dactylopiidae). As Dactylopiibacterium has not yet been cultured in the laboratory, metagenomes and metatranscriptomics have been key in revealing putative symbiont functions. Dactylopiibacterium is a nitrogen-fixing beta-proteobacterium that may be vertically transmitted and shows differential gene expression inside the cochineal depending on the tissue colonized. Here we found that all cochineal species tested had Dactylopiibacterium carminicum which has a highly conserved genome. All Dactylopiibacterium genomes analyzed had genes involved in nitrogen fixation and plant polymer degradation. Dactylopiibacterium genomes resemble those from free-living plant bacteria, some found as endophytes. Notably, we found here a new putative novel function where the bacteria may protect the insect from viruses, since all Dactylopiibacterium genomes contain CRISPRs with a spacer matching nucleopolyhedrovirus that affects insects.

Nasturtium leaf compounds, diphenyl disulfide and lyral, against Atta sexdens (Hymenoptera: Formicidae) and their symbiotic fungi.

Social insect pests, particularly leaf-cutting ants, present a considerable challenge in terms of control. Leaf-cutting ants are significant agricultural, forestry, and pasture pests, and understanding their behavior and defense mechanisms is essential for managing their colonies effectively. While toxic ant baits are a primary control method, the limited availability of effective insecticides and concerns over their hazardous nature has spurred the search for alternative solutions, particularly natural compounds, which aligns with the goals of forest certification groups. In the light of previous evidence demonstrating the efficacy of nasturtium leaves (Tropaeolum majus L. (Brassicales: Tropaeolaceae)) in suppressing leaf-cutting ant colonies, this study investigates 2 active components of nasturtium leaf extracts: diphenyl disulfide and lyral. We tested their impact on Atta sexdens (L.) (Hymenoptera: Formicidae), the most prevalent leaf-cutter ant species in Brazil, and their symbiotic fungus, Leucoagaricus gongylophorus (Möller) Singer (Agaricales: Agaricaceae). We conducted experiments with increasing concentrations of diphenyl disulfide and lyral, assessing their effects on the symbiotic fungus and on forager workers and gardeners of A. sexdens colonies. Our findings revealed no fungicidal activity, and ant mortality was minimal in both topical and ingestion bioassays with the exception of gardeners topically exposed to diphenyl sulfide. Furthermore, the compounds did not affect leaf ingestion, but diphenyl disulfide did increase interactions among foragers. These results suggest that neither diphenyl disulfide nor lyral are the primary contributors to the suppression of leaf-cutting ant colonies by nasturtium leaves. However, they may enhance the formicidal activity of other compounds present in nasturtium leaves.

Effects of arbuscular mycorrhizal fungi in the rhizosphere of two olive (Olea europaea) varieties Arbequina and Barnea under water deficit conditions.

One strategy to improve olive (Olea europaea ) tree drought tolerance is through the symbiosis of arbuscular mycorrhizal fungi (AMF), which helps alleviate water deficit through a combination of morphophysiological effects. Cuttings of olive varieties Arbequina (A) and Barnea (B) were grown with (+AMF) or without (-AMF) inoculum in the olive grove rhizosphere soil. One year after establishment, pots were exposed to four different water regimes: (1) control (100% of crop evapotranspiration); (2) short-period drought (20days); (3) long-period drought (25days); and (4) rewatering (R). To evaluate the influence of AMF on tolerance to water stress, stem water potential, stomatal conductance and the biomarkers for water deficit malondialdehyde, proline, soluble sugars, phenols, and flavonoids were evaluated at the end of the irrigation regimes. Stem water potential showed higher values in A(+) and B(+) in all water conditions, and the opposite was true for stomatal conductance. For proline and soluble sugars, the stem water potential trend is repeated with some exceptions. AMF inoculum spore communities from A(+ and -) and B(+ and -) were characterised at the morphospecies level in terms of richness and abundance. Certain morphospecies were identified as potential drought indicators. These results highlight that the benefits of symbiotic relationships between olive and native AMF can help to mitigate the effects of abiotic stress in soils affected by drought.

Desert plants, arbuscular mycorrhizal fungi and associated bacteria: Exploring the diversity and role of symbiosis under drought.

Desert plants, such as Agave tequilana, A. salmiana and Myrtillocactus geometrizans, can survive harsh environmental conditions partly due to their symbiotic relationships with microorganisms, including arbuscular mycorrhizal fungi (AMF). Interestingly, some of these fungi also harbour endosymbiotic bacteria. Our research focused on investigating the diversity of these AMFs and their associated bacteria in these plants growing in arid soil. We found that agaves have a threefold higher AMF colonization than M. geometrizans. Metabarcoding techniques revealed that the composition of AMF communities was primarily influenced by the plant host, while the bacterial communities were more affected by the specific plant compartment or niche they inhabited. We identified both known and novel endofungal bacterial taxa, including Burkholderiales, and confirmed their presence within AMF spores using multiphoton microscopy. Our study also explored the effects of drought on the symbiosis between A. tequilana and AMF. We discovered that the severity of drought conditions could modulate the strength of this symbiosis and its outcomes for the plant holobiont. Severe drought conditions prevented the formation of this symbiosis, while moderate drought conditions promoted it, thereby conferring drought tolerance in A. tequilana. This research sheds light on the diversity of AMF and associated bacteria in Crassulacean Acid Metabolism (CAM) plants and underscores the crucial role of drought as a factor modulating the symbiosis between A. tequilana and AMF. Further research is needed to understand the role of endofungal bacteria in this response.

Evolutionary déjà vu? A case of convergent evolution in an ant-plant association.

Obligatory ant-plant symbioses often appear to be single evolutionary shifts within particular ant lineages; however, convergence can be revealed once natural history observations are complemented with molecular phylogenetics. Here, we describe a remarkable example of convergent evolution in an ant-plant symbiotic system. Exclusively arboreal, Myrmelachista species can be generalized opportunists nesting in several plant species or obligately symbiotic, live-stem nesters of a narrow set of plant species. Instances of specialization within Myrmelachista are known from northern South America and throughout Middle America. In Middle America, a diverse radiation of specialists occupies understory treelets of lowland rainforests. The morphological and behavioural uniformity of specialists suggests that they form a monophyletic assemblage, diversifying after a single origin of specialization. Using ultraconserved element phylogenomics and ancestral state reconstructions, we show that shifts from opportunistic to obligately symbiotic evolved independently in South and Middle America. Furthermore, our analyses support a remarkable case of convergence within the Middle American radiation, with two independently evolved specialist clades, arising nearly simultaneously from putative opportunistic ancestors during the late Pliocene. This repeated evolution of a complex phenotype suggests similar mechanisms behind trait shifts from opportunists to specialists, generating further questions about the selective forces driving specialization.

Coevolutionary hotspots favour dispersal and fuel biodiversity in mutualistic landscapes under environmental changes.

Mutualistic interactions are key to sustaining Earth's biodiversity. Yet, we are only beginning to understand how coevolution in mutualistic assemblages can shape the distribution and persistence of species across landscapes. Here, we combine the geographic mosaic theory of coevolution with metacommunity dynamics to understand how geographically structured selection can shape patterns of richness, dispersal, extinction and persistence of mutualistic species. In this model, species may experience strong or weak reciprocal selection imposed by mutualisms within each patch (i.e. hotspots and coldspots, respectively). Using numerical simulations, we show that mutualistic coevolution leads to a concentration of species richness at hotspots. Such an effect occurs because hotspots sustain higher rates of colonization and lower rates of extinction than coldspots, whether the environment changes or not. Importantly, under environmental changes, coldspots fail to sustain a positive colonization-to-extinction balance. Rather, species persistence within coldspots relies on hotspots acting as biodiversity sources and enhancing population dispersal across the landscape. In fact, even a few hotspots in the landscape can fuel the spatial network of dispersal of populations in the metacommunity. Our study highlights that coevolutionary hotspots can act as biodiversity sources, favouring colonization and allowing species to expand their distribution across landscapes even in changing environments. This article is part of the theme issue 'Diversity-dependence of dispersal: interspecific interactions determine spatial dynamics'.

Negative density dependence characterizes mutualistic interactions between birds and fruiting plants across latitudes.

Negative density dependence (NDD) in biotic interactions of interference such as plant-plant competition, granivory and herbivory are well-documented mechanisms that promote species' coexistence in diverse plant communities worldwide. Here, we investigated the generality of a novel type of NDD mechanism that operates through the mutualistic interactions of frugivory and seed dispersal among fruit-eating birds and plants. By sampling community-wide frugivory interactions at high spatial and temporal resolution in Pennsylvania, Puerto Rico, Peru, Brazil and Argentina, we evaluated whether interaction frequencies between birds and fruit resources occurred more often (selection), as expected, or below expectations (under-utilization) set by the relative fruit abundance of the fruit resources of each plant species. Our models considered the influence of temporal scales of fruit availability and bird phylogeny and diets, revealing that NDD characterizes frugivory across communities. Irrespective of taxa or dietary guild, birds tended to select fruits of plant species that were proportionally rare in their communities, or that became rare following phenological fluctuations, while they mostly under-utilized abundant fruit resources. Our results demonstrate that negative density-dependence in frugivore-plant interactions provides a strong equalizing mechanism for the dispersal processes of fleshy-fruited plant species in temperate and tropical communities, likely contributing to building and sustaining plant diversity. This article is part of the theme issue 'Diversitydependence of dispersal: interspecific interactions determine spatial dynamics'.

Epigenetic control during root development and symbiosis.

The roots of plants play multiple functions that are essential for growth and development, including anchoring to the soil as well as water and nutrient acquisition. These underground organs exhibit the plasticity to modify their root system architecture in response to environmental cues, allowing adaptation to change in water and nutrient availability. In addition, roots enter in mutualistic interactions with soil microorganisms, for example, the root nodule symbiosis (RNS) established between a limited group of plants and nitrogen-fixing soil bacteria and the arbuscular mycorrhiza symbiosis involving most land plants and fungi of the Glomeromycetes phylum. In the past 20 years, genetic approaches allowed the identification and functional characterization of genes required for the specific programs of root development, root nodule, and arbuscular mycorrhiza symbioses. These genetic studies provided evidence that the program of the RNS recruited components of the arbuscular mycorrhiza symbiosis and the root developmental programs. The execution of these programs is strongly influenced by epigenetic changes-DNA methylation and histone post-translational modifications-that alter chromatin conformation modifying the expression of key genes. In this review, we summarize recent advances that highlight how DNA methylation and histone post-translational modifications, as well as chromatin remodeling factors and long noncoding RNAs, shape the root system architecture and allow the successful establishment of both root nodule and arbuscular mycorrhiza symbioses. We anticipate that the analysis of dynamic epigenetic changes and chromatin 3D structure in specific single cells or tissue types of root organs will illuminate our understanding of how root developmental and symbiotic programs are orchestrated, opening exciting questions and new perspectives to modulate agronomical and ecological traits linked to nutrient acquisition.