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BackgroundSpecialized interactions help structure communities, but persistence of specialized organisms is puzzling because a generalist can occupy more environments and partake in more beneficial interactions. The "Jack-of-all-trades is a master of none" hypothesis asserts that specialists persist because the fitness of a generalist utilizing a particular habitat is lower than that of a specialist adapted to that habitat. Yet, there are many reasons to expect that mutualists will generalize on partners.Plant-soil feedbacks help to structure plant and microbial communities, but how frequently are soil-based symbiotic mutualistic interactions sufficiently specialized to influence species distributions and community composition? To address this question, we quantified realized partner richness and phylogenetic breadth of four wild-grown native legumes (Lupinus bicolor, L. arboreus, Acmispon strigosus and A. heermannii) and performed inoculation trials to test the ability of two hosts (L. bicolor and A. strigosus) to nodulate (fundamental partner richness), benefit from (response specificity), and provide benefit to (effect specificity) 31 Bradyrhizobium genotypes.ResultsIn the wild, each Lupinus species hosted a broader genetic range of Bradyrhizobium than did either Acmispon species, suggesting that Acmispon species are more specialized. In the greenhouse, however, L. bicolor and A. strigosus did not differ in fundamental association specificity: all inoculated genotypes nodulated both hosts. Nevertheless, A. strigosus exhibited more specificity, i.e., greater variation in its response to, and effect on, Bradyrhizobium genotypes. Lupinus bicolor benefited from a broader range of genotypes but averaged less benefit from each. Both hosts obtained more fitness benefit from symbionts isolated from conspecific hosts; those symbionts in turn gained greater fitness benefit from hosts of the same species from which they were isolated.ConclusionsThis study affirmed two important tenets of evolutionary theory. First, as predicted by the Jack-of-all-trades is a master of none hypothesis, specialist A. strigosus obtained greater benefit from its beneficial symbionts than did generalist L. bicolor. Second, as predicted by coevolutionary theory, each test species performed better with partner genotypes isolated from conspecifics. Finally, positive fitness feedback between the tested hosts and symbionts suggests that positive plant-soil feedback could contribute to their patchy distributions in this system.

Aims: Domestication and crop breeding has improved plants for human use, but may have unintended consequences for traits that are not selected upon. Disruption in the mycorrhizal mutualism has been observed in crops; possibly due to breeding in fertilised soil. Little is known about whether the legume-rhizobia mutualism can be disrupted by domestication and crop evolution, despite the importance of symbiotic nitrogen fixation. We aimed to identify differences in mutualistic outcomes between five legume cultivars and their wild progenitors in terms of their reactions across varying nitrogen levels. Methods: With five greenhouse experiments, we characterised symbiosis traits in chickpea, lentil, pea, peanut, and soybean across a gradient of N fertilisation to characterise whether symbiosis traits differ context specifically between wild and domesticated lines. Results: At lower levels of N addition, wild soybean benefited more from rhizobia than domesticated soybean. Chickpea cultivars abandoned symbiosis at lower N than wild chickpea accessions. Chickpea cultivars reduced per-nodule colony forming units (CFU) in response to N addition more than wild chickpeas, but lentil cultivars reduced CFU less than lentil accessions. The lentil, pea, and peanut cultivars did not differ from their wild relatives in rhizobial benefit, nor in nodulation response to N addition. Conclusions: Differences in the regulation of the root nodule symbiosis are evident between domesticated and wild chickpea and soybean, but not lentil, pea, or peanut. This indicates that mutualism disruption—a decrease in the magnitude of the mutually symbiotic interaction—is a possible, but not necessary, consequence of domestication. [ABSTRACT FROM AUTHOR]

In mutualism, hosts select symbionts via partner choice and preferentially direct more resources to symbionts that provide greater benefits via sanctions. At the initiation of symbiosis, prior to resource exchange, it is not known how the presence of multiple symbiont options (i.e. the symbiont social environment) impacts partner choice outcomes. Furthermore, little research addresses whether hosts primarily discriminate among symbionts via sanctions, partner choice or a combination. We inoculated the legume, Acmispon wrangelianus, with 28 pairs of fluorescently labelled Mesorhizobium strains that vary continuously in quality as nitrogen-fixing symbionts. We find that hosts exert robust partner choice, which enhances their fitness. This partner choice is conditional such that a strain's success in initiating nodules is impacted by other strains in the social environment. This social genetic effect is as important as a strain's own genotype in determining nodulation and has both transitive (consistent) and intransitive (idiosyncratic) effects on the probability that a symbiont will form a nodule. Furthermore, both absolute and conditional partner choice act in concert with sanctions, among and within nodules. Thus, multiple forms of host discrimination act as a series of sieves that optimize host benefits and select for costly symbiont cooperation in mixed symbiont populations. [ABSTRACT FROM AUTHOR]

In mutualisms, variation at genes determining partner fitness provides the raw material upon which coevolutionary selection acts, setting the dynamics and pace of coevolution. However, we know little about variation in the effects of genes that underlie symbiotic fitness in natural mutualist populations. In some species of legumes that form root nodule symbioses with nitrogen‐fixing rhizobial bacteria, hosts secrete nodule‐specific cysteine‐rich (NCR) peptides that cause rhizobia to differentiate in the nodule environment. However, rhizobia can cleave NCR peptides through the expression of genes like the plasmid‐borne Host range restriction peptidase (hrrP), whose product degrades specific NCR peptides. Although hrrP activity can confer host exploitation by depressing host fitness and enhancing symbiont fitness, the effects of hrrP on symbiosis phenotypes depend strongly on the genotypes of the interacting partners. However, the effects of hrrP have yet to be characterised in a natural population context, so its contribution to variation in wild mutualist populations is unknown. To understand the distribution of effects of hrrP in wild rhizobia, we measured mutualism phenotypes conferred by hrrP in 12 wild Ensifer medicae strains. To evaluate context dependency of hrrP effects, we compared hrrP effects across two Medicago polymorpha host genotypes and across two experimental years for five E. medicae strains. We show for the first time in a natural population context that hrrP has a wide distribution of effect sizes for many mutualism traits, ranging from strongly positive to strongly negative. Furthermore, we show that hrrP effect size varies across host genotypes and experiment years, suggesting that researchers should be cautious about extrapolating the role of genes in natural populations from controlled laboratory studies of single genetic variants. [ABSTRACT FROM AUTHOR]

Although most invasive species engage in mutualism, we know little about how mutualism evolves as partners colonize novel environments. Selection on cooperation and standing genetic variation for mutualism traits may differ between a mutualism's invaded and native ranges, which could alter cooperation and coevolutionary dynamics. To test for such differences, we compare mutualism traits between invaded‐ and native‐range host‐symbiont genotype combinations of the weedy legume, Medicago polymorpha, and its nitrogen‐fixing rhizobium symbiont, Ensifer medicae, which have coinvaded North America. We find that mutualism benefits for plants are indistinguishable between invaded‐ and native‐range symbioses. However, rhizobia gain greater fitness from invaded‐range mutualisms than from native‐range mutualisms, and this enhancement of symbiont fecundity could increase the mutualism's spread by increasing symbiont availability during plant colonization. Furthermore, mutualism traits in invaded‐range symbioses show lower genetic variance and a simpler partitioning of genetic variance between host and symbiont sources, compared to native‐range symbioses. This suggests that biological invasion has reduced mutualists' potential to respond to coevolutionary selection. Additionally, rhizobia bearing a locus (hrrP) that can enhance symbiotic fitness have more exploitative phenotypes in invaded‐range than in native‐range symbioses. These findings highlight the impacts of biological invasion on the evolution of mutualistic interactions. [ABSTRACT FROM AUTHOR]

Students often struggle to connect concepts with evidence, sometimes because development of research skills has not been emphasized in their science courses. We developed a strategy and protocol to train high school students in research and experimental investigation of questions related to course material on legume biology. The richness of this subject matter allows for adaptations of our framework to address diverse areas of science, including principles in ecology, environmental science, agriculture, microbiology, and evolution. Our framework includes a hands-on classroom inquiry that investigates the symbiotic relationship between nitrogen-fixing rhizobial bacteria and legumes. This student-led, inquiry-based project employs an intellectually demanding, hands-on method of education to build critical research skills using an adaptable model and inexpensive materials. We also report positive student feedback from a post hoc survey to gauge student attitudes toward the activity and the effectiveness of this framework. [ABSTRACT FROM AUTHOR]

Mutualistic interactions can strongly influence species invasions, as the inability to form successful mutualisms in an exotic range could hamper a host's invasion success. This barrier to invasion may be overcome if an invader either forms novel mutualistic associations or finds and associates with familiar mutualists in the exotic range. Here, we ask (1) does the community of rhizobial mutualists associated with invasive legumes in their exotic range overlap with that of local native legumes and (2) can any differences be explained by fundamental incompatibilities with particular rhizobial genotypes? To address these questions, we first characterized the rhizobial communities naturally associating with three invasive and six native legumes growing in the San Francisco Bay Area. We then conducted a greenhouse experiment to test whether the invasive legume could nodulate with any of a broad array of rhizobia found in their exotic range. There was little overlap between the Bradyrhizobium communities associated with wild-grown invasive and native legumes, yet the invasive legumes could nodulate with a broad range of rhizobial strains under greenhouse conditions. These observations suggest that under field conditions in their exotic range, these invasive legumes are not currently associating with the mutualists of local native legumes, despite their potential to form such associations. However, the promiscuity with which these invading legumes can form mutualistic associations could be an important factor early in the invasion process if mutualist scarcity limits range expansion. Overall, the observation that invasive legumes have a community of rhizobia distinct from that of native legumes, despite their ability to associate with many rhizobial strains, challenges existing assumptions about how invading species obtain their mutualists. These results can therefore inform current and future efforts to prevent and remove invasive species. [ABSTRACT FROM AUTHOR]

Although adaptive plant population divergence across contrasting soil conditions is often driven by abiotic soil factors, natural enemies may also contribute. Cryptic matching to the native soil color is a form of defensive camouflage that seeds can use to avoid detection by seed predators., The legume Acmispon wrangelianus occurs across a variety of gray-green serpentine soils and brown nonserpentine soils. Quantitative digital image analysis of seed and soil colors was used to test whether genetically based seed color is a closer match to the color of the native soil than to the color of other nearby soils., Lineages bear seeds that more closely match the color of their native serpentine or nonserpentine soil type than the opposing soil type. Further, even within a soil type, lineages bear seeds with a closer color match to the soil at their native site than to other sites., The striking concordance between seed and native soil color suggests that natural selection for locally camouflaged seed color morphs, probably driven by seed predators, may maintain adaptive divergence in pigmentation, despite the opportunity for migration between soil environments. [ABSTRACT FROM AUTHOR]

Specialization and concomitant trade-offs are assumed to underlie the non-neutral coexistence of lineages. Trade-offs across heterogeneous environments can promote diversity by preventing competitive exclusion. However, the importance of trade-offs in maintaining diversity in natural microbial assemblages is unclear, as trade-offs are frequently not detected in artificial evolution experiments. Stressful conditions associated with patches of heavy-metal enriched serpentine soils provide excellent opportunities for examining how heterogeneity may foster genetic diversity. Using a spatially replicated design, we demonstrate that rhizobium bacteria symbiotic with legumes inhabiting contrasting serpentine and nonserpentine soils exhibit a trade-off between a genotype's nickel tolerance and its ability to replicate rapidly. Furthermore, we detected adaptive divergence in rhizobial assemblages across soil type heterogeneity at multiple sites, suggesting that this trade-off may promote the coexistence of phenotypically distinct bacterial lineages. Trade-offs and adaptive divergence may be important factors maintaining the tremendous diversity within natural assemblages of bacteria. [ABSTRACT FROM AUTHOR]