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1. When does mutualism offer a competitive advantage? A game-theoretic analysis of host–host competition in mutualism

   https://doi.org/10.1093/aobpla/plac010  

   Halloway, Abdel H; Heath, Katy D; McNickle, Gordon G (April 2022, AoB PLANTS)

   Beaulieu, Jeremy (Ed.)

   Abstract Due to their non-motile nature, plants rely heavily on mutualistic interactions to obtain resources and carry out services. One key mutualism is the plant–microbial mutualism in which a plant trades away carbon to a microbial partner for nutrients like nitrogen and phosphorous. Plants show much variation in the use of this partnership from the individual level to entire lineages depending upon ecological, evolutionary and environmental context. We sought to determine how this context dependency could result in the promotion, exclusion or coexistence of the microbial mutualism by asking if and when the partnership provided a competitive advantage to the plant. To that end, we created a 2 × 2 evolutionary game in which plants could either be a mutualist and pair with a microbe or be a non-mutualist and forgo the partnership. Our model includes both frequency dependence and density dependence, which gives us the eco-evolutionary dynamics of mutualism evolution. As in all models, mutualism only evolved if it could offer a competitive advantage and its net benefit was positive. However, surprisingly the model reveals the possibility of coexistence between mutualist and non-mutualist genotypes due to competition between mutualists over the microbially obtained nutrient. Specifically, frequency dependence of host strategies can make the microbial symbiont less beneficial if the microbially derived resources are shared, a phenomenon that increasingly reduces the frequency of mutualism as the density of competitors increases. In essence, ecological competition can act as a hindrance to mutualism evolution. We go on to discuss basic experiments that can be done to test and falsify our hypotheses. 

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2. Recurrent mutualism breakdown events in a legume rhizobia metapopulation

   https://doi.org/10.1098/rspb.2019.2549  

   Gano-Cohen, Kelsey A.; Wendlandt, Camille E.; Al Moussawi, Khadija; Stokes, Peter J.; Quides, Kenjiro W.; Weisberg, Alexandra J.; Chang, Jeff. H.; Sachs, Joel L. (January 2020, Proceedings of the Royal Society B: Biological Sciences)

   Bacterial mutualists generate major fitness benefits for eukaryotes, reshaping the host phenotype and its interactions with the environment. Yet, microbial mutualist populations are predicted to generate mutants that defect from providing costly services to hosts while maintaining the capacity to exploit host resources. Here, we examined the mutualist service of symbiotic nitrogen fixation in a metapopulation of root-nodulating Bradyrhizobium spp . that associate with the native legume Acmispon strigosus . We quantified mutualism traits of 85 Bradyrhizobium isolates gathered from a 700 km transect in California spanning 10 sampled A. strigosus populations. We clonally inoculated each Bradyrhizobium isolate onto A. strigosus hosts and quantified nodulation capacity and net effects of infection, including host growth and isotopic nitrogen concentration. Six Bradyrhizobium isolates from five populations were categorized as ineffective because they formed nodules but did not enhance host growth via nitrogen fixation. Six additional isolates from three populations failed to form root nodules. Phylogenetic reconstruction inferred two types of mutualism breakdown, including three to four independent losses of effectiveness and five losses of nodulation capacity on A. strigosus . The evolutionary and genomic drivers of these mutualism breakdown events remain poorly understood. 

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3. The geographic footprint of mutualism: How mutualists influence species' range limits

   https://doi.org/10.1002/ecm.1558  

   Fowler, Joshua C.; Donald, Marion L.; Bronstein, Judith L.; Miller, Tom E. X. (January 2023, Ecological Monographs)

   Abstract Understanding mechanisms that generate range limits is central to knowing why species are found where they are and how they will respond to environmental change. There is growing awareness that biotic interactions play an important role in generating range limits. However, current theory and data overwhelmingly focus on abiotic drivers and antagonistic interactions. Here we explore the effect that mutualists have on their partner's range limits: the geographic “footprint” of mutualism. This footprint arises from two general processes: modification of a partner's niche through environment‐dependent fitness effects and, for a subset of mutualisms, dispersal opportunities that lead suitable habitats to be filled. We developed a conceptual framework that organizes different footprints of mutualism and the underlying mechanisms that shape them, and evaluated supporting empirical evidence from the primary literature. In the available literature, we found that the fitness benefits and dispersal opportunities provided by mutualism can extend species' ranges; conversely, the absence of mutualism can constrain species from otherwise suitable regions of their range. Most studies found that the footprint of mutualism is driven by changes in the frequency of mutualist partners from range core to range edge, whereas fewer found changes in interaction outcomes, the diversity of partners, or varying sensitivities of fitness to the effects of mutualists. We discuss these findings with respect to specialization, dependence, and intimacy of mutualism. Much remains unknown about the geographic footprint of mutualisms, leaving fruitful areas for future work. A particularly important future direction is to explore the role of mutualism during range shifts under global change, including the promotion of shifts at leading edges and persistence at trailing edges. 

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4. Coevolution and dependency influence resistance of mutualists to exploitation

   https://doi.org/10.3389/fevo.2024.1113963  

   Vidal, Mayra C.; Agarwal, Renuka; Segraves, Kari A. (March 2024, Frontiers in Ecology and Evolution)

   A long-standing problem in the study of mutualism is to understand the effects of non-mutualistic community members that exploit the benefits of mutualism without offering commodities in exchange (i.e., ‘exploiters’). Mutualisms are continually challenged by exploiters and their persistence may depend on the costliness of exploitation or on adaptations that allow mutualists to avoid the negative effects of exploiters. Coevolution could lead to changes in mutualists and exploiters that allow mutualisms to persist. Although coevolution is considered essential for mutualism persistence and resistance to disturbance, we have yet to obtain direct experimental evidence of the role of coevolution in resistance to exploitation. Additionally, resistance to exploitation via coevolutionary processes might vary with the degree of dependency between mutualistic partners, as facultative mutualisms are thought to be under weaker coevolutionary selection than obligate mutualisms. Here, we conducted an experimental evolution study using a synthetic yeast mutualism to test how coevolution in facultative and obligate mutualisms affects their resistance to exploitation. We found that naïve facultative mutualisms were more likely to breakdown under exploitation than naïve obligate mutualisms. After 15 weeks of coevolution, both facultative and obligate evolved mutualists were more likely to survive exploitation than naïve mutualists when we reassembled mutualist communities. Additionally, coevolved exploiters were more likely to survive with mutualists, whereas naïve exploiters frequently went extinct. These results suggest that coevolution between mutualists and exploiters can lead to mutualism persistence, potentially explaining why exploitation is ubiquitous but rarely associated with mutualism breakdown. 

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5. Extreme specificity in obligate mutualism—A role for competition?

   https://doi.org/10.1002/ece3.11628  

   Agarwal, Renuka; Althoff, David_M (June 2024, Ecology and Evolution)

   Abstract Obligate mutualisms, reciprocally obligate beneficial interactions, are some of the most important mutualisms on the planet, providing the basis for the evolution of the eukaryotic cell, the formation and persistence of terrestrial ecosystems and the establishment and expansion of coral reefs. In addition, these mutualisms can also lead to the diversification of interacting partner species. Accompanying this diversification is a general pattern of a high degree of specificity among interacting partner species. A survey of obligate mutualisms demonstrates that greater than half of these systems have only one or two mutualist species on each side of the interaction. This is in stark contrast to facultative mutualisms that can have dozens of interacting mutualist species. We posit that the high degree of specificity in obligate mutualisms is driven by competition within obligate mutualist guilds that limits species richness. Competition may be particularly potent in these mutualisms because mutualistic partners are totally dependent on each other's fitness gains, which may fuel interspecific competition. Theory and the limited number of empirical studies testing for the role of competition in determining specificity suggest that competition may be an important force that fuels the high degree of specificity. Further empirical research is needed to dissect the relative roles of trait complementarity, mutualism regulation, and competition among mutualist guild members in determining mutualism specificity at local scales. 

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