Tripartite mutualisms as models for understanding plant–microbial interactions

Afkhami, Michelle E.; Almeida, Brianna K.; Hernández, Damián; Kiesewetter, Kasey N.; Revillini, Daniel

doi:10.1016/j.pbi.2020.02.003

Cited by 44 publications

(45 citation statements)

References 52 publications

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“…We posit two factors may lead to synergistic selection: the importance of the trait in acquiring resources later traded to mutualist partners and complementarity of partner‐provided benefits (Afkhami et al, 2014, 2020). For host resource‐acquisition traits, we expect that they will be subject to synergistic selection when the same resource is provided to all partners: in these cases, selection can favour trait values that increase the size of the resource ‘pie’.…”

Section: Discussionmentioning

confidence: 99%

Multiple Mutualism Effects generate synergistic selection and strengthen fitness alignment in the interaction between legumes, rhizobia and mycorrhizal fungi

2021

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Nearly all organisms participate in multiple mutualisms, and complementarity within these complex interactions can result in synergistic fitness effects. However, it remains largely untested how multiple mutualisms impact eco‐evolutionary dynamics in interacting species. We tested how multiple microbial mutualists—N‐fixing bacteria and mycorrrhizal fungi—affected selection and heritability of traits in their shared host plant (Medicago truncatula), as well as fitness alignment between partners. Our results demonstrate for the first time that multiple mutualisms synergistically affect the selection and heritability of host traits and enhance fitness alignment between mutualists. Specifically, we found interaction with multiple microbial symbionts doubled the strength of natural selection on a plant architectural trait, resulted in 2‐ to 3‐fold higher heritability of plant reproductive success, and more than doubled fitness alignment between N‐fixing bacteria and plants. These findings show synergism generated by multiple mutualisms extends to key components of microevolutionary change, emphasising the importance of multiple mutualism effects on evolutionary trajectories.

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Section: Discussionmentioning

confidence: 99%

Multiple Mutualism Effects generate synergistic selection and strengthen fitness alignment in the interaction between legumes, rhizobia and mycorrhizal fungi

2021

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“…Multiple mutualists can have significant, synergistic effects on heritability and selection for host traits, and can substantially influence fitness alignment within mutualisms. Taken together with the well-established fact that organisms often interact with multiple mutualists (Afkhami et al 2014(Afkhami et al , 2020, these outcomes demonstrate the importance of multiple mutualist effects for evolutionary trajectories of organisms and their beneficial interactions. In our opinion, there are at least three types of studies that will be valuable for furthering our understanding of multispecies mutualisms' roles in eco-evolutionary dynamics.…”

Section: Conclusion and Prospectsmentioning

confidence: 78%

“…We posit two factors may lead to synergistic selection: the importance of the trait in acquiring resources later traded to mutualist partners (e.g., traits involved in carbon acquisition, when C-based rewards are provided to microbial partners) and complementarity of partnerprovided rewards (Afkhami et al 2014(Afkhami et al , 2020. For host resource-acquisition traits, we expect that they will be subject to synergistic selection when the same resource is provided to all partners: in these cases, there should be selection favoring trait values that increase the size of the resource 'pie.'…”

Section: Selection In Multiple Mutualisms Much Of the Work On Selectmentioning

confidence: 99%

“…Field common garden studies with tractable partners would be especially valuable. Third, to link complementarity of partner mutualists (Afkhami et al 2014(Afkhami et al , 2020 with synergistic selection, studies factorially manipulating within-versus across-guild multiple mutualisms and measuring selection and complementarity are needed. Collectively, studies like these will make meaningful progress in understanding the eco-evolutionary consequences of multispecies mutualisms.…”

Section: Conclusion and Prospectsmentioning

confidence: 99%

“…MMEs are common, and often generate nonadditive effects on performance or fitness of shared hosts (Afkhami et al 2014) as well as on the molecular phenotypes underpinning these effects (Afkhami & Stinchcombe 2016;Palakurty et al 2018). In particular, MMEs, unlike effects of multiple predators (or competitors), can synergistically increase fitness of shared hosts if each partner species provides distinct and complementary rewards (e.g., rhizobia and mycorrhizal fungi providing nitrogen and phosphorus, respectively, to a host plant; Afkhami et al 2020). Although nonadditive effects can alter ecological and evolutionary dynamics of species in ways that cannot be predicted from studies of pairwise interactions, our understanding of how they do so remains limited.…”

Section: Introductionmentioning

confidence: 99%

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Multiple Mutualist Effects generate synergistic selection and strengthen fitness alignment in a tripartite interaction between legumes, rhizobia, and mycorrhizal fungi

Afkhami

Friesen

Stinchcombe

2021

Preprint

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Nearly all organisms interact with multiple mutualists, and complementarity within these complex interactions can result in synergistic fitness effects. However, it remains largely untested how multiple mutualists impact eco-evolutionary dynamics. We tested how multiple microbial mutualists-- N-fixing bacteria and mycorrrhizal fungi-- affected selection and heritability in their shared host plant (Medicago truncatula), as well as fitness alignment between partners. Our results demonstrate for the first time that multispecies mutualisms synergistically affect selection and heritability of host traits and enhance fitness alignment between mutualists. Specifically, we found that multiple mutualists doubled the strength of selection on a plant architectural trait, resulted in 2-3-fold higher heritability of reproductive success, and more than doubled the strength of fitness alignment between N-fixing bacteria and plants. Taken together, these findings show that synergism generated by multiple mutualisms extends to key components of microevolutionary change, and emphasizes the importance of multiple mutualist effects in understanding evolutionary trajectories.

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Contrasting effects of nectar yeasts on the reproduction of Mediterranean plant species

Vega

Albaladejo

Álvarez‐Pérez

et al. 2022

American J of Botany

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Premise Yeasts are often present in floral nectar and can influence plant fitness directly (independently of pollinators) or indirectly by influencing pollinator visitation and behavior. However, few studies have assessed the effect of nectar yeasts on plant reproductive success or compared effects across different plant species, limiting our understanding of the relative impact of direct vs. indirect effects. Methods We inoculated the nectar of six plant species in the field with the cosmopolitan yeast Metschnikowia reukaufii to analyze the direct and indirect effects on female reproductive success over 2 years. The pollinator assemblage for each species was recorded during both flowering years. Results Direct yeast effects on female fecundity were statistically nonsignificant for all plant species. There were significant indirect, pollinator‐mediated effects on fruit production and seed mass for the two species pollinated almost exclusively by bumblebees or hawkmoths, with the direction of the effects differing for the quantity‐ and quality‐related fitness components. There were no consistent effects of the yeast on maternal fecundity for any of the species with diverse pollinator assemblages. Conclusions Effects of M. reukaufii on plant reproduction ranged from negative to neutral or positive depending on the plant species. The among‐species variation in the indirect effects of nectar yeasts on plant pollination could reflect variation in the pollinator community, the specific microbes colonizing the nectar, and the order of microbial infection (priority effects), determining potential species interactions. Elucidating the nature of these multitrophic plant–pollinator–microbe interactions is important to understand complex processes underlying plant pollination.

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Tripartite mutualisms as models for understanding plant–microbial interactions

Cited by 44 publications

References 52 publications

Multiple Mutualism Effects generate synergistic selection and strengthen fitness alignment in the interaction between legumes, rhizobia and mycorrhizal fungi

Multiple Mutualism Effects generate synergistic selection and strengthen fitness alignment in the interaction between legumes, rhizobia and mycorrhizal fungi

Multiple Mutualist Effects generate synergistic selection and strengthen fitness alignment in a tripartite interaction between legumes, rhizobia, and mycorrhizal fungi

Contrasting effects of nectar yeasts on the reproduction of Mediterranean plant species

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