Showing papers by "James D. Bever published in 2014"

Synergism and context dependency of interactions between arbuscular mycorrhizal fungi and rhizobia with a prairie legume

Abstract: Biotic interactions play primary roles in major theories of the distribution and abundance of species, yet the nature of these biotic interactions can depend upon the larger ecological community. Leguminous plants, for example, commonly associate with both arbuscular mycorrhizal fungi (AMF) and rhizobia bacteria, and the pairwise interactions may depend upon the presence or identity of the third partner. To determine if the dynamics of plant-AMF and plant-rhizobia interactions are affected by the alternate symbiont, we manipulated the presence and identity of each symbiont, as well as levels of the nutrients supplied by each symbiont (nitrogen and phosphorus), on the growth of prairie legume Amorpha canescens. We found strong synergistic effects of AMF and rhizobia inoculation on plant biomass production that were independent of nutrient levels. AMF and rhizobia responses were each influenced by the other, but not in the same direction. AMF infection increased root nodule number and mass, but rhizobia inoculation decreased AMF hyphal colonization of roots. The relative benefits of each combination of symbionts depended upon phosphorus level. The effect of nitrogen was also contingent on the biotic environment where nitrogen addition decreased nodulation, but this decrease was reduced with coinfection by AMF. Our results demonstrate a strong contingency on the co-occurrence of AMF and rhizobia for the long-term fitness of A. canescens, and suggest that the belowground community is critical for the success of this species in tallgrass prairies.

Coexistence and relative abundance in plant communities are determined by feedbacks when the scale of feedback and dispersal is local

Abstract: 1. Negative plant-soil feedback occurs when the presence of an individual of a particular species at a particular site decreases the relative success of individuals of the same species compared to those other species at that site. This effect favors heterospecifics thereby facilitating coexistence and maintaining diversity. Empirical work has demonstrated that the average strengths of these feedbacks correlate with the relative abundance of species within a community, suggesting that feedbacks are an important driver of plant community composition. Understanding what factors contribute to the generation of this relationship is necessary for diagnosing the dynamic forces that maintain diversity in plant communities. 2. We used a spatially explicit, individual-based computer simulation to test the effects of dispersal distance, the size of feedback neighbourhoods, the strength of pairwise feedbacks and community wide variation of feedbacks, community richness, as well as life-history differences on the dependence of relative abundance on strength of feedback. 3. We found a positive dependence of relative abundance of a species on its average feedback for local scale dispersal and feedback. However, we found that the strength of this dependence decreased as either the spatial scale of dispersal and/or the spatial scale of feedback increased. We also found that for spatially local (i.e. relatively small) scale interaction and dispersal, as the mean strength of feedbacks in the community becomes less negative, the greater the increase in abundance produced by a comparable increase in species-specific average feedback. We found that life-history differences such as mortality rate did not generate a pattern with abundance, nor did they affect the relationship between abundance and average feedback. 4. Synthesis. Our results support the claim that empirical observations of a positive correlation between relative abundance and strength of average feedback serves as evidence that local scale negative feedbacks play a prominent role in structuring plant communities. We also identify that this relationship depends upon local scale plant dispersal and feedback which generates clumping and magnifies the negative feedbacks.

Ecological dynamics and complex interactions of Agrobacterium megaplasmids.

Abstract: As with many pathogenic bacteria, agrobacterial plant pathogens carry most of their virulence functions on a horizontally transmissible genetic element. The tumor-inducing (Ti) plasmid encodes the majority of virulence functions for the crown gall agent Agrobacterium tumefaciens. This includes the vir genes which drive genetic transformation of host cells and the catabolic genes needed to utilize the opines produced by infected plants. The Ti plasmid also encodes, an opine-dependent quorum sensing system that tightly regulates Ti plasmid copy number and its conjugal transfer to other agrobacteria. Many natural agrobacteria are avirulent, lacking the Ti plasmid. The burden of harboring the Ti plasmid depends on the environmental context. Away from diseased hosts, plasmid costs are low but the benefit of the plasmid is also absent. Consequently, plasmidless genotypes are favored. On infected plants the costs of the Ti plasmid can be very high, but balanced by the opine benefits, locally favoring plasmid bearing cells. Cheating derivatives which do not incur virulence costs but can benefit from opines are favored on infected plants and in most other environments, and these are frequently isolated from nature. Many agrobacteria also harbor an At plasmid which can stably coexist with a Ti plasmid. At plasmid genes are less well characterized but in general facilitate metabolic activities in the rhizosphere and bulk soil, such as the ability to breakdown plant exudates. Examination of A. tumefaciens C58, revealed that harboring it’s At plasmid is much more costly than harboring it’s Ti plasmid, but conversely the At plasmid is extremely difficult to cure. The interactions between these co-resident plasmids are complex, and depend on environmental context. However, the presence of a Ti plasmid appears to mitigate At plasmid costs, consistent with the high frequency with which they are found together.

The Coexistence of Hosts with Different Abilities to Discriminate against Cheater Partners: An Evolutionary Game-Theory Approach

Abstract: Evolutionary theory predicts that mutualisms based on the reciprocal exchange of costly services should be susceptible to exploitation by cheaters. Consistent with theory, both cheating and discrimination against cheaters are ubiquitous features of mutualisms. Several recent studies have confirmed that host species differ in the extent that they are able to discriminate against cheaters, suggesting that cheating may be stabilized by the existence of susceptible hosts (dubbed “givers”). We use an evolutionary game-theoretical approach to demonstrate how discriminating and giver hosts associating with mutualist and cheater partners can coexist. Discriminators drive the proportion of cheaters below a critical threshold, at which point there is no benefit to investing resources into discrimination. This promotes givers, who benefit from mutualists but allow cheater populations to rebound. We then apply this model to the plant-mycorrhizal mutualism and demonstrate it is one mechanism for generating hos...

Non-additive costs and interactions alter the competitive dynamics of co-occurring ecologically distinct plasmids.

Abstract: Plasmids play an important role in shaping bacterial evolution and adaptation to heterogeneous environments. As modular genetic elements that are often conjugative, the selective pressures that act on plasmid-borne genes are distinct from those that act on the chromosome. Many bacteria are co-infected by multiple plasmids that impart niche-specific phenotypes. Thus, in addition to host–plasmid dynamics, interactions between co-infecting plasmids are likely to be important drivers of plasmid population dynamics, evolution and ecology. Agrobacterium tumefaciens is a facultative plant pathogen that commonly harbours two distinct megaplasmids. Virulence depends on the presence of the tumour-inducing (Ti) plasmid, with benefits that are primarily restricted to the disease environment. Here, we demonstrate that a second megaplasmid, the At plasmid, confers a competitive advantage in the rhizosphere. To assess the individual and interactive costs of these plasmids, we generated four isogenic derivatives: plasmidless, pAt only, pTi only and pAtpTi, and performed pairwise competitions under carbon-limiting conditions. These studies reveal a low cost to the virulence plasmid when outside of the disease environment, and a strikingly high cost to the At plasmid. In addition, the costs of pAt and pTi in the same host were significantly lower than predicted based on single plasmid costs, signifying the first demonstration of non-additivity between naturally occurring co-resident plasmids. Based on these empirically demonstrated costs and benefits, we developed a resource–consumer model to generate predictions about the frequencies of these genotypes in relevant environments, showing that non-additivity between co-residing plasmids allows for their stable coexistence across environments.

Integration of clustering and multidimensional scaling to determine phylogenetic trees as spherical phylograms visualized in 3 dimensions

Abstract: Phylogenetic analysis is commonly used to analyze genetic sequence data from fungal communities, while ordination and clustering techniques commonly are used to analyze sequence data from bacterial communities. However, few studies have attempted to link these two independent approaches. In this paper, we propose a method, which we call spherical phylogram (SP), to display the phylogenetic tree within the clustering and visualization result from a pipeline called DACIDR. In comparison with traditional tree display methods, the correlations between the tree and the clustering can be observed directly. In addition, we propose an algorithm called interpolative joining (IJ) to construct and visualize the SP in 3D space. In the experiments, we used the sum of branch lengths to quantify the general fit between the clustering and the phylogenetic tree in SP and Mantel tests to determine how well the same grouping of sequences was preserved between the clustering and the SP. Our results show that DACIDR has a classification accuracy that is similar to a phylogenetic tree generated using a multiple sequence alignment, while having much lower computational cost.

Joint Evolution of Kin Recognition and Cooperation in Spatially Structured Rhizobium Populations

Abstract: In the face of costs, cooperative interactions maintained over evolutionary time present a central question in biology. What forces maintain this cooperation? Two potential ways to explain this problem are spatially structured environments (kin selection) and kin-recognition (directed benefits). In a two-locus population genetic model, we investigated the relative roles of spatial structure and kin recognition in the maintenance of cooperation among rhizobia within the rhizobia-legume mutualism. In the case where the cooperative and kin recognition loci are independently inherited, spatial structure alone maintains cooperation, while kin recognition decreases the equilibrium frequency of cooperators. In the case of co-inheritance, spatial structure remains a stronger force, but kin recognition can transiently increase the frequency of cooperators. Our results suggest that spatial structure can be a dominant force in maintaining cooperation in rhizobium populations, providing a mechanism for maintaining the mutualistic nodulation trait. Further, our model generates unique and testable predictions that could be evaluated empirically within the legume-rhizobium mutualism.

Dispersal and spatial heterogeneity allow coexistence between enemies and protective mutualists.

Abstract: Protective mutualisms, where a symbiont reduces the negative effects of another species on a shared host, represent a common type of species interaction in natural communities, yet it is still unclear what ecological conditions might favor their emergence. Studies suggest that the initial evolution of protective mutualists might involve closely related pathogenic variants with similar life histories, but different competitive abilities and impacts on host fitness. We derive a model to evaluate this hypothesis and show that, in general, a protective variant cannot spread from rarity or exclude a more pathogenic strain. While the conditions allowing mutualist invasion are more likely with increased environmental productivity, they still depend on initial densities in the invaded patch exceeding a threshold, highlighting the likely importance of spatial structure and demographic stochasticity. Using a numerical simulation approach, we show that regional coexistence is in fact possible in an explicitly spatial system and that, under some circumstances, the mutualist population can exclude the enemy. More broadly, the establishment of protective mutualists may be favored when there are other life-history differences from more pathogenic symbionts, such as vertical transmission or additional direct benefits to hosts.