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Species interactions are a unifying theme in ecology and evolution. Both fields are currently moving beyond their historical focus on isolated pairwise relationships to understand how ecological communities affect focal interactions. Additional species can modify both the number of interactions and the fitness consequences of each interaction (i.e., selection). Although only selection affects the evolution of the focal interaction, the two are often conflated, limiting our understanding of the evolution of multispecies interactions. We manipulated aboveground herbivory on the legume Medicago lupulina in the field and quantified its effect on number of symbionts and the per-symbiont impact on plant performance in two belowground symbioses: mutualistic rhizobia bacteria (Ensifer meliloti) and parasitic root-knot nematodes (Meloidogyne hapla). We found that herbivores modified the number of rhizobia nodules, as well as the benefit per nodule. However, each effect was specific to a distinct herbivory regime: natural herbivory affected nodule number, whereas leafhoppers (Cicadellidae) weakened the per nodule benefit. We did not detect any effect of herbivory on nematode gall number or the cost of infection. Our data demonstrate that distinguishing between symbiont number from the fitness consequences of symbiosis is crucial to accurately infer how pairwise interactions will evolve in a community.

Eusocial insect societies possess complex multilevel disease defences, including individual level protection conferred by physical (e.g. cuticle) and immunological obstacles and colony level protection mediated by collective behaviours (social immunity). It remains unclear whether and how these two levels of disease protection are related to one another in jointly driving colonies’ susceptibility to disease. Here, we examine whether a relationship exists between individual worker survival after exposure to a fungal pathogen (a proxy for immunity) and corpse removal (a colony level social immunity metric) in the acorn ant Temnothorax curvispinosus. Since behavioural avoidance is the first line of defence against infection, we also tested whether individual ants exhibited parasite avoidance behaviour during exploration and whether colonies exhibit avoidance behaviour during foraging. We found that individual level and colony level immunity were negatively correlated: colonies that removed corpses more rapidly contained workers with weaker individual defences. We did not detect parasite avoidance behaviour by individual workers or whole colonies, nor were these two factors related. These data suggest that individual immunity and social immunity may trade off, regulating overall parasite protection. Alternatively, optimized social immunity at the colony level may compensate for disease vulnerability to infection at the individual level, and thus provide a protective benefit in overall colony defence in the absence of pathogen avoidance.

Priority effects shape the assembly of free-living communities and host-associated communities. However, the current literature does not fully incorporate two features of host-symbiont interactions, correlated host responses to multiple symbionts and ontogenetic changes in host responses to symbionts, leading to an incomplete picture of the role of priority effects in host-associated communities. We factorially manipulated the inoculation timing of two plant symbionts (mutualistic rhizobia bacteria and parasitic root-knot nematodes) and tested how host age at arrival, arrival order, and arrival synchrony affected symbiont colonization success in the model legume Medicago truncatula. We found that host age, arrival order, and arrival synchrony significantly affected colonization of one or both symbionts. Host age at arrival only affected nematodes but not rhizobia: younger plants were more heavily infected than older plants. By contrast, arrival order only affected rhizobia but not nematodes: plants formed more rhizobia nodules when rhizobia arrived before nematodes. Finally, synchronous arrival decreased colonization both symbionts, an effect that depended on host age. Our results demonstrate that priority effects compromise the host's ability to control colonization by two major symbionts and suggest that the role of correlated host responses and host ontogeny in the assembly of host-associated communities deserve further attention.

Evidence is accumulating that the soil microbiome—the community of microorganisms living in soils—has a major effect on plant traits and fitness. However, most work to date has taken place under controlled laboratory conditions and has not experimentally disentangled the effect of the soil microbiome on plant performance from the effects of key endosymbiotic constituents. As a result, it is difficult to extrapolate from existing data to understand the role of the soil microbiome in natural plant populations. To address this gap, we performed a field experiment using the black medick Medicago lupulina to test how the soil microbiome influences plant performance and colonization by two root endosymbionts (the mutualistic nitrogen‐fixing bacteria Ensifer spp. and the parasitic root‐knot nematode Meloidogyne hapla) under natural conditions. We inoculated all plants with nitrogen‐fixing bacteria and factorially manipulated the soil microbiome and nematode infection. We found that plants grown in microbe‐depleted soil exhibit greater mortality, but that among the survivors, there was no effect of the soil microbiome on plant performance (shoot biomass, root biomass, or shoot‐to‐root ratio). The soil microbiome also impacted parasitic nematode infection and affected colonization by mutualistic nitrogen‐fixing bacteria in a plant genotype‐dependent manner, increasing colonization in some plant genotypes and decreasing it in others. Our results demonstrate the soil microbiome has complex effects on plant–endosymbiont interactions and may be critical for survival under natural conditions., We show that the soil microbial community affects survival and interactions with two major root endosymbionts (nitrogen‐fixing bacteria and parasitic root‐knot nematodes) in the field in the legume Medicago lupulina. Our experiment demonstrates that the significant fitness consequences of host‐associated microbial communities that have been observed in the laboratory persist under natural conditions, and suggests that the role of soil microbial communities in mediating key endosymbioses merits future research.

Despite widespread evidence that biological invasion influences both the biotic and abiotic soil environments, the extent to which these two pathways underpin the effects of invasion on plant traits and performance remains unknown. Leveraging a long-term (14-year) field experiment, we show that an allelochemical-producing invader affects plants through biotic mechanisms, altering the soil fungal community composition, with no apparent shifts in soil nutrient availability. Changes in belowground fungal communities resulted in high costs of nutrient uptake for native perennials and a shift in plant traits linked to their water and nutrient use efficiencies. Some plants in the invaded community compensate for the disruption of nutritional symbionts and reduced nutrient provisioning by sanctioning more nitrogen to photosynthesis and expending more water, which demonstrates a trade-off in trait investment. For the first time, we show that the disruption of belowground nutritional symbionts can drive plants towards alternative regions of their trait space in order to maintain water and nutrient economics.

Premise We developed a novel low-cost method to visually phenotype belowground structures in the plant rhizosphere. We devised the method introduced here to address the difficulties encountered growing plants in seed germination pouches for long-term experiments and the high cost of other mini-rhizotron alternatives. Methods and results The method described here took inspiration from homemade ant farms commonly used as an educational tool in elementary schools. Using compact disc (CD) cases, we developed mini-rhizotrons for use in the field and laboratory using the burclover Medicago lupulina. Conclusions Our method combines the benefits of pots and germination pouches. In CD mini-rhizotrons, plants grew significantly larger than in germination pouches, and unlike pots, it is possible to measure roots without destructive sampling. Our protocol is a cheaper, widely available alternative to more destructive methods, which could facilitate the study of belowground phenotypes and processes by scientists with fewer resources.

Evolutionary ecologists often seek to identify the mechanisms maintaining intraspecific variation. In social animals, whole groups can exhibit between-group differences in their collective traits. We examined whether negative frequency-dependent selection (that is, a rare-type advantage) could help to maintain between-group variation. We engineered neighbourhoods of social spider colonies bearing bold or shy foraging phenotypes and monitored their fecundity in situ. We found that bold colonies enjoyed a rare-type advantage that is lost as the frequency of bold colonies in a neighbourhood increases. The success of shy colonies was not frequency dependent. These dynamics seem to be driven by a foraging advantage of bold colonies that is lost in bold neighbourhoods because prey become scarce, and shy colonies perform better than bold colonies under low-resource conditions. Thus, to understand selection on collective traits, it is insufficient to examine groups in isolation. The phenotypic environment in which groups reside and compete must also be considered.