Biology subjects

Doyle, R. T.

Publications and source records attributed to Doyle, R. T..

4 recordsLinked to original sources

bioRxiv2026

Negative frequency-dependent selection maintains partner quality variation in a keystone nutritional mutualism

Mutualisms, interactions that benefit both partners, are critical for promoting biodiversity and ecosystem resiliency, yet are considered evolutionarily unstable and vulnerable to global change. Understanding how genetic variation in mutualisms is maintained is key to predicting their future persistence and explaining their long evolutionary history. While theory addresses factors maintaining variation in partner quality (the fitness benefits partners provide), few studies have experimentally tested these mechanisms. Here, we experimentally evolved multiple replicate populations of rhizobia, nitrogen-fixing mutualists of legumes, varying in partner quality under contrasting environments: nitrogen (N)-supplemented or N-free conditions, with or without host plants. After one year of rhizobial evolution, we quantified selection on partner quality across environments and evaluated resulting changes in mutualism traits and population-level genetic diversity. Strikingly, selection on partner quality was population-dependent: high-quality strains were favoured when initially rare but disfavoured when common, revealing negative-frequency dependent dynamics that can maintain variation. Although neither nitrogen-supplementation nor host presence directly imposed selection, both were critical for preserving genetic diversity in rhizobia populations - fuel for ongoing evolution. By demonstrating negative-frequency dependent selection in the legume-rhizobium mutualism, our study reveals a dynamic more akin to antagonistic interactions than traditionally assumed. This overlooked mechanism may be the key to explaining the ecological and evolutionary persistence of mutualisms under changing environments. Significance StatementMutualisms are central to biodiversity, yet their stability is puzzling because the mechanisms thought to stabilize them tend to eliminate the genetic variation needed for continued adaptation, even though partners in nature show striking variation in quality. In an experimental evolution study of a keystone plant-microbe mutualism (legume-rhizobium symbiosis), we found that negative frequency-dependent selection allows high- and low-quality symbionts to coexist: high-quality strains are favoured only when rare. Environmental factors such as nitrogen addition or host presence did not alter which partners were selected, but they helped maintain genetic diversity needed for future adaptation. Our findings reveal an overlooked mechanism that stabilizes mutualisms and explain how these interactions can remain resilient under changing environmental conditions.

evolutionary biology↗

bioRxiv2025

Crop-specific and microbially-mediated impacts of alternative agricultural amendments on plant performance

Rising fertilizer costs and dwindling freshwater supplies are driving interest in alternative agricultural amendments such as biosolids and reclaimed water. While these inputs can promote crop growth, they also contain persistent contaminants like PFAS, which may affect plants directly or indirectly via changes to plant-associated microbiomes. The extent and mechanisms of these effects remain poorly understood, particularly across crops with differing functional traits. We conducted two greenhouse experiments to evaluate the direct and microbially mediated effects of biosolid and reclaimed water amendments spiked with increasing contaminant concentrations on lettuce (Lactuca sativa), radish (Raphanus sativus), and green pea (Pisum sativum). Peas exhibited pronounced negative responses to biosolids, including reduced germination, survival, and biomass, which scaled with contaminant concentration and coincided with visible pathogen infection. Lettuce and radish showed minimal impact, suggesting that plant functional traits--such as symbiotic capacity and nutrient-dependent immune regulation--may mediate susceptibility to contaminant-induced stress. Soil microbiome diversity and composition were altered in a crop- and amendment-specific manner, but microbiomes shaped by prior exposure had limited effects on pea performance when transferred to new plants in the absence of ongoing stressors. These findings suggest that current soil conditions and active plant-microbiome interactions may outweigh legacy microbiome effects. Overall, our study provides a novel framework for evaluating the risks and benefits of wastewater-derived amendments, emphasizing the importance of functional trait variation in predicting plant responses to contaminants and guiding sustainable agricultural practices.

plant biology↗

bioRxiv2024

Plasmid transmission dynamics and evolution of partner quality in a natural population of Rhizobium leguminosarum

Many bacterial traits important to host-microbe symbiosis are determined by genes carried on extrachromosomal replicons such as plasmids, chromids, and integrative and conjugative elements. Multiple such replicons often coexist within a single cell and, due to horizontal mobility, have patterns of variation and evolutionary histories that are distinct from each other and from the bacterial chromosome. In nitrogen-fixing Rhizobium, genes carried on multiple plasmids make up almost 50% of the genome, are necessary for the formation of symbiosis, and underlie bacterial traits including host plant benefits. Thus the genomics and transmission of plasmids in Rhizobium underlie the ecology and evolution of this important model symbiont. Here we leverage a natural population of clover-associated Rhizobium in which partner quality has declined in response to long-term nitrogen fertilization. We use 62 novel, reference-quality genomes to characterize 257 replicons in the plasmidome and study their genomics and transmission patterns. We find that, of the four most frequent plasmid types, two (types II & III) have more stable size, larger core genomes, and track the chromosomal phylogeny (display more vertical transmission), while others (types I & IV - the symbiosis plasmid, or pSym) vary substantially in size, shared gene content, and have phylogenies consistent with frequent horizontal transmission. We also find differentiation in pSym subtypes driven by long-term nitrogen fertilization. Our results highlight the variation in plasmid transmission dynamics within a single symbiont and implicate plasmid horizontal transmission in the evolution of partner quality. IMPORTANCEUnderstanding how bacterial genes move through natural populations is critical for understanding how bacterial traits evolve. The nitrogen-fixing bacterium Rhizobium leguminosarum lives in symbiosis with plants and is a model for studying how gene transmission from one cell to another on mobile genetic elements called plasmids impacts the evolution of bacteria and plants. Here we characterize the genomes of a natural bacterial population, then use novel approaches to show that mechanisms of plasmid gene transmission varies across multiple plasmid types possessed by R. leguminosarum. We find that changes in plasmid genes are associated with the decline of symbiotic partner quality in strains isolated from environments undergoing long-term fertilization. Together, these results underscore the importance of plasmid evolution in shaping ecosystem processes like nitrogen cycling. Our study provides a framework for probing the plasmid dynamics within natural bacterial populations and how plasmid transmission affects genetic diversity and ecological interactions in bacteria.

genomics↗

bioRxiv2023

Drivers of population dynamics of at-risk populations change with pathogen arrival

Successful wildlife conservation in an era of rapid global change requires understanding determinants of species population abundance and growth. However, when populations are faced with novel stressors, factors associated with healthy and growing populations can change, necessitating a shift in conservation strategies. For example, emerging infectious diseases can cause conditions previously beneficial or neutral to host populations to increase disease impacts. Here, we paired a population dataset of 265 colonies of the federally endangered Indiana bat (Myotis sodalis) with 50.7 logger-years of environmental data to explore factors that affected colony response to white-nose syndrome (WNS), an emerging fungal disease. We found wide variation in colony responses to WNS, ranging from extirpation to stabilization and persistence. Simulating future population dynamics suggests that most extirpations have already occurred, as the pathogen has been present for several years in most colonies, and that small colonies were more susceptible to extirpation than large ones. Further, while temperature and humidity conditions of hibernacula appeared unassociated with Indiana bat colony growth prior to WNS, extirpation risk following pathogen arrival was elevated in colonies that used colder and wetter hibernacula. Additionally, rates of decline were greater in colder hibernacula, opposite the association for a sympatric bat species. Overall, this study illustrates that emerging infectious diseases can change the factors associated with host population abundance and optimal growth, including through novel environmental associations, which can vary across host species. Consideration of these shifting associations and intrinsic differences between impacted host species will be essential to successful species conservation.

ecology↗