Lutz Becks

Photosymbiosis has evolved multiple times independently in ciliates. However, these associations can be antagonized by shifts in environmental parameters that impose stress on the host, necessitating the evolution of mechanisms to contend with this stress and to control the symbiont population. To investigate whether convergent strategies have evolved among algae-bearing ciliates in the class Oligohymenophorea, we imposed light stress on three host species that represent at least two independent evolutionary origins of photosymbiosis and measured their cellular responses. Under high light, all three species experienced an initial drop in host cell density which recovered to levels commensurate with those under low-light conditions as they decreased their symbiont loads. We then performed a comparative transcriptomic study to investigate whether a core set of genes exists that is involved in this response. Thirty-one gene families possess differentially expressed transcripts across all three species that included the upregulation C1 and S28 class peptidases, genes involved in ROS mitigation, and a gene with potential involvement in mitochondrial remodeling associated with changes in algal symbiont load. We additionally found downregulation in Dicer , which could mitigate the processing of algal transcripts by the hosts’ RNAi machinery that are freed upon algal digestion, and downregulation of motor proteins that may reflect changes in the host’s swimming behaviors and transport of intracellular vesicles in response to light. The 31 gene families are present and widespread in non-symbiotic oligohymenophoreans, illustrating that a pre-existing genetic toolkit exists in this clade that helps explain how it is predisposed to evolving photosymbioses.

Biological communities are complex, dynamic systems that underpin ecosystem functionality, yet their long-term dynamics and predictability remain poorly understood. Understanding how Darwinian evolution shapes these systems through eco-evolutionary feedback is a central challenge in ecology and evolution. Experimental studies using simplified microbial assemblages have yielded important insights into the ecological principles governing community states. However, an important knowledge gap is how selection within member species drives changes of community state in multispecies systems. Here, we present a four-year evolution experiment involving a 23-species synthetic bacterial community propagated in two environments: a control medium and the same medium supplemented with the antibiotic streptomycin. Through combined analyses of community composition and genome evolution, we quantified the temporal changes in species abundances and the evolutionary trajectories of individual community members. The extended duration of the experiment enabled the detection of adaptive mutations and community state shifts that occur only over long evolutionary timescales. We show that community dynamics are environment dependent and reproducible across replicates and that evolution of streptomycin resistance in a previously streptomycin-sensitive species on its own can induce abrupt community state shifts. Our results provide a direct demonstration of eco-evolutionary feedbacks within a multispecies community, revealing how a single adaptive mutation can reorganize complex ecological networks.

Microbial communities frequently encounter recurrent antibiotic disturbance, yet how ecological, evolutionary, and environmental processes jointly shape the response remains unresolved. Here we experimentally disentangle these mechanisms using a 23-species bacterial community exposed to ampicillin pulses with pre-pulse and resistance priming. Pre-pulse priming preconditioned community composition toward resistant taxa, reducing compositional change during the main pulse. Resistance priming was the dominant determinant of community response, buffering compositional change, relaxing selection, and altering gene expression. This buffering arose from both evolution of higher resistance and accelerated ampicillin detoxification by a dominant degrader, which transiently reduced antibiotic effects and favoured non-degrading taxa. Yet buffering did not translate into better recovery: because resistance was coupled to competitive dominance, diversity remained comparable to or below that of ancestral communities, and dominance was reinforced. Together, we show that antibiotic history reshapes microbial disturbance response through coupled eco-evolutionary and environmental feedbacks, generating a trade-off between resistance and recovery.

Testing inter‐ and intraspecific competition is essential for understanding the processes that maintain diversity within communities and populations. Pairwise growth assays are well‐established methods to study the outcome of competition between bacterial genotypes or species. However, distinguishing bacterial competitors in coculture remains a major challenge due to their small cell size, similar cell morphology, and often large population sizes. Current approaches are either labour intensive and require prior morphological and sequence‐based characterisation or genetic modification of the bacteria. We present a simple assay that tracks the relative abundances of two competing bacterial species or genotypes of the same species through transient staining of one competitor with a fluorescent dye. The use of a transient dye relieves prior genetic characterisation or modification. Our approach uses a sample‐dependent threshold evaluation for the fluorescent intensity, enabling the quantification of bacterial frequencies over generations. The method provides high accuracy for tracking competing genotypes and species. The outcome of competition often depends on frequency‐dependent fitness effects and/or environmental variables. Therefore, our method tests across different initial abundances and can also assess the role of a biotic interaction (presence/absence of a predator) on the outcome of competition. Our method presents a simple and high‐throughput assay for competition. Absence of genetic modifications and applicability to little characterised competitors make it particularly useful for assays involving bacterial isolates from evolving populations.

Recent studies have revealed bacterial genome-wide evolution to be complex and dynamic even in a constant environment, characterized by the emergence of new clades competing or temporarily coexisting as each clade undergoes evolutionary change. Previous studies on predator-prey dynamics tracking simple ecological and phenotypic metrics have shown predation to fundamentally alter prey evolution, facilitating defense evolution followed by coevolution and frequency dependent selection between defended and undefended prey genotypes. Here we sought to consolidate these fields by examining genome-wide evolution in five bacterial prey species separately subjected to long-term evolution under ciliate predation. We hypothesized that the presence of predation could change the pattern of clonal dynamics, for example, by more frequently producing selective sweeps if predation-defense-related mutations are under strong selection. For all species, we found mutational signals of prey adaptation, with phenotypic data and genomic mutation targets demonstrating changes in composition between the experimental treatments. Intriguingly, despite higher variant counts, overall temporal clade dynamics across the coevolved prey species were strikingly similar to those of bacteria evolving alone, with constant emergence, competition and quasi-stable coexistence of clades. This study shows that long-term molecular evolution in bacterial prey under predation is more interesting and less predictable than we might expect based on existing coevolutionary theories.

Microbial communities frequently encounter recurrent antibiotic disturbance, yet how ecological, evolutionary, and environmental processes jointly shape community responses remains unresolved. Here, we use priming to describe the history-dependent effect whereby prior exposure alters the response to a subsequent disturbance. Using a 23-species bacterial community exposed to sequential ampicillin pulses, we examined two dimensions of priming. The ecological dimension was manipulated by exposing assembled communities to an antibiotic pre-pulse that could alter species composition before a common high-dose pulse. The evolutionary dimension was manipulated by experimentally evolving individual species for increased ampicillin resistance before community assembly. Community-level pre-pulse exposure shifted composition toward resistant taxa before the main disturbance, reducing subsequent compositional change. Prior resistance evolution had the strongest effect on community dynamics, buffering compositional change during the main pulse, relaxing subsequent selection, and altering community-wide gene expression. This buffering arose from both increased resistance within species and accelerated ampicillin detoxification by a dominant degrader, which transiently reduced antibiotic exposure and promoted the persistence of non-degrading taxa. However, greater resistance did not improve recovery. Because resistance was coupled to competitive dominance, diversity after disturbance remained similar to or lower than in ancestral communities, whereas dominant taxa became further enriched. Together, our results show that antibiotic exposure history reshapes microbial disturbance responses through interacting eco-evolutionary and environmental feedbacks. These feedbacks increase resistance to recurrent disturbance but can constrain recovery, revealing a trade-off between resistance and diversity restoration.

A cornerstone of biology is that species interactions drive evolution of niche divergence, thereby maintaining biodiversity. Yet controlled experiments consistently find evolution of competitive-ability differences instead, creating a fundamental discrepancy with patterns observed in nature. Here, we investigated the role of environmental heterogeneity, a major determinant on niche availability, on evolution of species interactions. Integrating theoretical models with experimental evolution in freshwater algal communities, we tracked the real-time evolution of coexistence mechanisms. In homogeneous environments, we found that although species consistently converged in resource use, the divergence in competitive-ability differences led to competitive exclusion. Conversely, in heterogeneous environments, species first evolved increased niche differences, which transiently stabilized coexistence before the communities converged to long-term, stable coexistence via both small niche and competitive-ability differences. Our study provides direct evidence that environmental heterogeneity determines whether evolution of species coexistence proceeds through niche or competitive-ability differences. It highlights that understanding the ecological context can help to understand and predict the evolutionary pathways that sustain biodiversity.

Predicting species coexistence and community assembly is a central goal in ecology. Traditional methods, based on the effect of one species on another (e.g., Lotka-Volterra competition model), are sensitive to environmental context. This is because they ignore the fundamental processes that can be applied across environments. While mechanistic approaches offer promise, empirical tests remain rare. Here, we integrate a mechanistic consumer-resource model with the growth of 12 phytoplankton species in monoculture over a range of nitrate, ammonium or phosphorous concentrations. We find that the mechanistic approach accurately predicts the composition of 960 communities across species richness and resource conditions. We confirm by simulations, species competing for substitutable resources (nitrate vs. ammonium) exhibit greater diversity than those competing for essential resources (nitrate vs. phosphorus), especially when initial species richness is high. This is because, in competition for essential resources, each species is likely to consume less of the resource that is more limiting to its growth, which violates the mechanistic rule of coexistence that states that each species must consume more of the resource that more limit it. Our study highlights the power of the mechanistic approach in understanding and predicting species loss across environments and, ultimately, mitigating its pace.

Rapid changes driven by the Anthropocene—including shifts in climate, nutrients, habitats, and species composition—are causing severe biodiversity loss while creating new ecological opportunities. The balance between short-term ecological shifts in realized niches and long-term evolutionary changes in fundamental niches determines diversification. In the Anthropocene, however, this balance is unstable, as environmental turnover often outpaces adaptive evolution. Processes such as interaction-network rewiring, mutualism loss or emergence, and microbiome-mediated plasticity can hinder or promote diversification. Identifying when opportunities persist, drive fundamental niche evolution, and enable biodiversity to withstand or recover from rapid global change requires a predictive framework linking ecological dynamics, evolutionary mechanisms, and host–microbiome interactions.