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1. Experimental evolution can enhance benefits of rhizobia to novel legume hosts

   https://doi.org/10.1098/rspb.2021.0812  

   Quides, Kenjiro W.; Weisberg, Alexandra J.; Trinh, Jerry; Salaheldine, Fathi; Cardenas, Paola; Lee, Hsu-Han; Jariwala, Ruchi; Chang, Jeff H.; Sachs, Joel L. (May 2021, Proceedings of the Royal Society B: Biological Sciences)

   null (Ed.)

   Legumes preferentially associate with and reward beneficial rhizobia in root nodules, but the processes by which rhizobia evolve to provide benefits to novel hosts remain poorly understood. Using cycles of in planta and in vitro evolution, we experimentally simulated lifestyles where rhizobia repeatedly interact with novel plant genotypes with which they initially provide negligible benefits. Using a full-factorial replicated design, we independently evolved two rhizobia strains in associations with each of two Lotus japonicus genotypes that vary in regulation of nodule formation. We evaluated phenotypic evolution of rhizobia by quantifying fitness, growth effects and histological features on hosts, and molecular evolution via genome resequencing. Rhizobia evolved enhanced host benefits and caused changes in nodule development in one of the four host–symbiont combinations, that appeared to be driven by reduced costs during symbiosis, rather than increased nitrogen fixation. Descendant populations included genetic changes that could alter rhizobial infection or proliferation in host tissues, but lack of evidence for fixation of these mutations weakens the results. Evolution of enhanced rhizobial benefits occurred only in a subset of experiments, suggesting a role for host–symbiont genotype interactions in mediating the evolution of enhanced benefits from symbionts. 

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2. Managing Friends and Foes: Sanctioning Mutualists in Mixed‐Infection Nodules Trades off With Defense Against Antagonists

   https://doi.org/10.1111/eva.70064  

   Wendlandt, Camille E; Basu, Saumik; Montoya, Angeliqua P; Roberts, Paige; Stewart, Justin D; Coffin, Allison B; Crowder, David W; Kiers, E Toby; Porter, Stephanie S (January 2025, Evolutionary Applications)

   ABSTRACT Successful plant growth requires plants to minimize harm from antagonists and maximize benefit from mutualists. However, these outcomes may be difficult to achieve simultaneously, since plant defenses activated in response to antagonists can compromise mutualism function, and plant resources allocated to defense may trade off with resources allocated to managing mutualists. Here, we investigate how antagonist attack affects plant ability to manage mutualists with sanctions, in which a plant rewards cooperative mutualists and/or punishes uncooperative mutualists. We studied interactions among wild and domesticated pea plants, pea aphids, an aphid‐vectored virus (Pea Enation Mosaic Virus, PEMV), and mutualistic rhizobial bacteria that fix nitrogen in root nodules. Using isogenic rhizobial strains that differ in their ability to fix nitrogen and express contrasting fluorescent proteins, we found that peas demonstrated sanctions in both singly‐infected nodules and mixed‐infection nodules containing both strains. However, the plant's ability to manage mutualists in mixed‐infection nodules traded off with its ability to defend against antagonists: when plants were attacked by aphids, they stopped sanctioning within mixed‐infection nodules, and plants that exerted stricter sanctions within nodules during aphid attack accumulated higher levels of the aphid‐vectored virus, PEMV. Our findings suggest that plants engaged in defense against antagonists suffer a reduced ability to select for the most beneficial symbionts in mixed‐infection tissues. Mixed‐infection tissues may be relatively common in this mutualism, and reduced plant sanctions in these tissues could provide a refuge for uncooperative mutualists and compromise the benefit that plants obtain from mutualistic symbionts during antagonist attack. Understanding the conflicting selective pressures plants face in complex biotic environments will be crucial for breeding crop varieties that can maximize benefits from mutualists even when they encounter antagonists. 

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3. Horizontal transmission enables flexible associations with locally adapted symbiont strains in deep-sea hydrothermal vent symbioses

   https://doi.org/10.1073/pnas.2115608119  

   Breusing, Corinna; Genetti, Maximilian; Russell, Shelbi L.; Corbett-Detig, Russell B.; Beinart, Roxanne A. (April 2022, Proceedings of the National Academy of Sciences)

   Symbiont specificity, both at the phylotype and strain level, can have profound consequences for host ecology and evolution. However, except for insights from a few model symbiosis systems, the degree of partner fidelity and the influence of host versus environmental factors on symbiont composition are still poorly understood. Nutritional symbioses between invertebrate animals and chemosynthetic bacteria at deep-sea hydrothermal vents are examples of relatively selective associations, where hosts affiliate only with particular, environmentally acquired phylotypes of gammaproteobacterial or campylobacterial symbionts. In hydrothermal vent snails of the sister genera Alviniconcha and Ifremeria , this phylotype specificity has been shown to play a role in habitat distribution and partitioning among different holobiont species. However, it is currently unknown if fidelity goes beyond species-level associations and influences genetic structuring, connectivity, and habitat adaptation of holobiont populations. We used metagenomic analyses to assess sequence variation in hosts and symbionts and identify correlations with geographic and environmental factors. Our analyses indicate that host populations are not differentiated across an ∼800-km gradient, while symbiont populations are clearly structured between vent locations due to a combination of neutral and selective processes. Overall, these results suggest that host individuals flexibly associate with locally adapted strains of their specific symbiont phylotypes, which supports a long-standing but untested paradigm of the benefits of horizontal transmission. Symbiont strain flexibility in these snails likely enables host populations to exploit a range of habitat conditions, which might favor widespread genetic connectivity and ecological resilience unless physical dispersal barriers are present. 

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4. Synergy, complexity, and the dirty, dirty cheats of the world

   https://doi.org/10.1111/brv.70041  

   Koop, Jennifer_A_H; Blackstone, Neil_W (May 2025, Biological Reviews)

   ABSTRACT Studies of symbiosis employ the term “parasitism” to connote different sorts of relationships. Within the context of mutualistic symbioses, parasites are otherwise cooperative individuals or strains that appropriate a disproportionate amount of the synergistic products. In the context of antagonistic symbioses, there is no pretence of cooperation, and instead parasites are defined as individuals or strains that derive fitness benefits at a fitness cost to their hosts. In both cases, parasitism is selected for at the lower level (that of the individual symbiont) but selected against at the higher level (the group of symbionts in a single host). Despite these similarities, these different sorts of parasitism likely evolve by different pathways. Once a host–symbiont relationship initiates, if functional synergy is lacking, the relationship will remain exploitative, although parasites may differ in their detrimental effects on the host and the higher‐level unit. If functional synergy is present, however, cooperation may develop with benefits for both host and symbionts (i.e. mutualism). Nevertheless, parasites may still evolve from within these incipient relationships when individuals or strains of symbionts act parasitically by defecting from the common good to further their selfish replication. Levels‐of‐selection dynamics thus underlie both forms of parasitism, but only in the case of latent functional synergy can true symbiotic complexity at the higher level emerge. 

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5. How host-microbiome/holobiont evolution depends on whether the microbiome affects host lifespan or fecundity

   https://doi.org/10.1093/jeb/voae127  

   Brown, Alexandra L; Koskella, Britt; Boots, Mike (January 2025, Journal of Evolutionary Biology)

   Li_Richter, Xiang-Yi; Jain, Kavita (Ed.)

   Abstract There is overwhelming evidence that the microbiome can be important to host physiology and fitness. As such, there is interest in and some theoretical work on understanding when hosts and microbiomes (co)evolve so that microbes benefit hosts and hosts favour beneficial microbes. However, the outcome of evolution likely depends on how microbes benefit hosts. Here, we use adaptive dynamics to investigate how host and symbiont evolution depend on whether symbionts increase host lifespan or host reproduction in a simple model of host and symbiont dynamics. In addition, we investigate 2 ways hosts release (and transmit) symbionts: by releasing symbionts steadily during their lifetime or by releasing them at reproduction, potentially increasing symbionts’ chances of infecting the host’s offspring. The former is strict horizontal transmission, whereas the latter is also a form of indirect or “pseudovertical” transmission. Our first key result is that the evolution of symbionts that benefit host fecundity requires pseudovertical transmission, while the evolution of symbionts that benefit host lifespan does not. Furthermore, our second key result is that when investing in host benefits is costly to the free-living symbiont stage, intermediate levels of pseudovertical transmission are needed for selection to favour beneficial symbionts. This is true regardless of fitness effects because release at reproduction increases the free-living symbiont population, which increases competition for hosts. Consequently, hosts could evolve away from traits that favour beneficial symbionts. Generally, our work emphasizes the importance of different forms of vertical transmission and fitness benefits in host, microbiome, and holobiont evolution as highlighted by our prediction that the evolution of fecundity-increasing symbionts requires parent-to-offspring transmission. 

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