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Abreu, C. I.

Publications and source records attributed to Abreu, C. I..

7 recordsLinked to original sources

Order invariance of fitness makes evolution predictable despite strong history-dependent effects

Environmental change is ubiquitous in nature, yet understanding its effect on the predictability of evolution remains a challenge. Previous work in microbes has shown that growth and fitness in a particular environment can depend strongly on the environments encountered previously. If such history-dependent effects are large, then any sequence of environments must be thought of as unique, and even a modest number of environments could generate a combinatorially large number of evolutionary paths. This would make evolution in changing environments difficult to predict. Here, we use cycles of three environments, which is the smallest number of environments which allow for comparisons of different environmental orderings -- X [->] Y [->] Z [->] X vs X [->] Z [->] Y [->] X -- to empirically test how environmental order affects the fitness of S. cerevisiae mutants. We measured the fitness of ~900 adaptive mutants in distinct three-environment cycles, and find large history-dependent effects which cause fitness in individual environmental components to differ drastically across the two directions of the cycle. However, these effects tend to compensate for each other, resulting in similar overall fitness across the whole cycle. This is true even when we specifically conduct experimental evolution in both directions of the same three-environment cycle. Of the ~450 mutants we isolated, only a small number of strains showed higher fitness in the direction in which they evolved. By splitting the contribution of each environment on fitness into its effect on the current and next component, we show that the invariance of overall fitness to environment order emerges because the effect of an environment on the next component is largely independent of the identity of the subsequent component, and can be captured by an additive model. Despite this general pattern of compensation, we do find instances of non-additivity, some of which are partly due to history-dependent effects lasting beyond two growth components. Overall, these results suggest that despite large history-dependent effects, fitness across a sequence of environments can be surprisingly predictable.

evolutionary biology↗

Strong environmental memory revealed by experimental evolution in static and fluctuating environments

Evolution in a static environment, such as a laboratory setting with constant and uniform conditions, often proceeds via large-effect beneficial mutations that may become maladaptive in other environments. Conversely, natural settings require populations to endure environmental fluctuations. A sensible assumption is that the fitness of a lineage in a fluctuating environment is the time-average of its fitness over the sequence of static conditions it encounters. However, transitions between conditions may pose entirely new challenges, which could cause deviations from this time-average. To test this, we tracked hundreds of thousands of barcoded yeast lineages evolving in static and fluctuating conditions and subsequently isolated 900 mutants for pooled fitness assays in 15 environments. We find that fitness in fluctuating environments indeed often deviates from the expectation based on static components, leading to fitness non-additivity. Moreover, closer examination reveals that fitness in one component of a fluctuating environment is often strongly influenced by the previous component. We show that this environmental memory is especially common for mutants with high variance in fitness across tested environments, even if the components of the focal fluctuating environment are excluded from this variance. We employ a simple mathematical model and whole-genome sequencing to propose mechanisms underlying this effect, including lag time evolution and sensing mutations. Our results demonstrate that environmental fluctuations have large impacts on fitness and suggest that variance in static environments can explain these impacts.

evolutionary biology↗

Warmer temperatures favor slower-growing bacteria in natural marine communities

Earths life-sustaining oceans harbor diverse bacterial communities that display varying composition across time and space. While particular patterns of variation have been linked to a range of factors, unifying rules are lacking, preventing the prediction of future changes. Here, analyzing the distribution of fast- and slow-growing bacteria in ocean datasets spanning seasons, latitude, and depth, we show that higher seawater temperatures universally favor slower-growing taxa, in agreement with theoretical predictions. Our results explain why slow growers dominate at the ocean surface, during summer, and near the tropics, and provide a framework to understand how bacterial communities will change in a warmer world.

ecology↗

Environmental fluctuations reshape an unexpected diversity-disturbance relationship in a microbial community

Environmental disturbances have long been theorized to play a significant role in shaping the diversity and composition of ecosystems1,2. However, fundamental limitations in our ability to specify the characteristics of a disturbance in the field and laboratory have produced an inconsistent picture of diversity-disturbance relationships (DDRs) that shape the structure of ecosystems3. Here, using a recently developed continuous culture system with tunable environmental control4, we decomposed a dilution disturbance into intensity and fluctuation components5,6, and tested their effects on the diversity of a soil-derived bacterial community across hundreds of replicate cultures. We observed an unexpected U-shaped relationship between community diversity and disturbance intensity in the absence of fluctuations, an observation counter to classical intuition. Adding fluctuations erased the U-shape and increased community diversity across all disturbance intensities. All of these results are well-captured by a Monod consumer resource model, which further reveals how U-shaped DDRs emerge based on a novel "niche flip" mechanism in which competitive outcomes flip and coexistence regimes subsequently collapse at intermediate disturbance levels. Broadly, our results demonstrate how distinct features of an environmental disturbance can interact in complex ways to govern ecosystem assembly and produce all the major classes of DDRs, without invoking other organizational principles. With these findings, we construct a unifying framework that reconciles the disparate DDRs observed in nature, and propose strategies for predictively reshaping the compositional complexity of microbiomes and other ecosystems.

bioengineering↗

Higher Temperatures Generically Favor Slower-Growing Bacterial Species in Multispecies Communities

Temperature is among the cardinal environmental variables which determine the composition and function of microbial communities. Many culture-independent studies have characterized communities that are affected by changing temperatures, either due to seasonal cycles1-3, long-term warming4-6, or latitudinal/elevational gradients7-8. However, a predictive understanding of how microbial communities respond to such changes in temperature is still lacking, partly because it is not obvious which aspects of microbial physiology determine whether a species should benefit from temperature alteration. Here, we incorporate how microbial growth rates change with temperature to a modified Lotka-Volterra competition model9, and predict that higher temperatures should generically favor slower-growing species in a bacterial community. We experimentally confirm this prediction in pairwise cocultures assembled from a diverse set of species, and we show that these changes to pairwise outcomes with temperature are also predictive of changing outcomes in three-species communities, suggesting our theory may propagate to more complex assemblages. Our results demonstrate that it is possible to predict how bacterial communities will shift with temperature knowing only the growth rates of the community members. These results provide a testable hypothesis for future studies of more complex, natural communities, and we hope that this work will help bridge the gap between ecological theory and the complex dynamics observed in metagenomic surveys.

ecology↗

Emergence of alternative stable states in microbial communities in a fluctuating environment

The effect of environmental fluctuations is a major question in ecology. While it is widely accepted that fluctuations and other types of disturbances can increase biodiversity, we have only a limited understanding of the circumstances in which other types of outcomes can occur in a fluctuating environment. Here we explore this question with laboratory microcosms, using cocultures of two bacterial species, P. putida and P. veronii. At low dilution rates we observe competitive exclusion of P. veronii, whereas at high dilution rates we observe competitive exclusion of P. putida. When the dilution rate alternates between high and low, we do not observe coexistence between the species, but rather alternative stable states, in which only one species survives and initial species fractions determine the identity of the surviving species. The Lotka-Volterra model with a fluctuating mortality rate predicts that this outcome is independent of the timing of the fluctuations, and that the time-averaged mortality would also lead to alternative stable states, a prediction that we confirm experimentally. Other pairs of species can coexist in a fluctuating environment, and again consistent with the model we observe coexistence in the time-averaged dilution rate. We find a similar time-averaging result holds in a three-species community, highlighting that simple linear models can in some cases provide powerful insight into how communities will respond to environmental fluctuations.

ecology↗

Mortality causes universal changes in microbial community composition

All organisms are sensitive to the abiotic environment, and a deteriorating environment can lead to extinction. However, survival in a multispecies community also depends upon inter-species interactions, and some species may even be favored by a harsh environment that impairs competitors. A deteriorating environment can thus cause surprising transitions in community composition. Here, we combine theory and laboratory microcosms to develop a predictive understanding of how simple multispecies communities change under added mortality, a parameter that represents environmental harshness. In order to explain changes in a multispecies microbial system across a mortality gradient, we examine its members pairwise interactions. We find that increasing mortality favors the faster grower, confirming a prediction of simple models. Furthermore, if the slower grower outcompetes the faster grower in environments with low or no added mortality, the competitive outcome can reverse as mortality increases. We find that this tradeoff between growth rate and competitive ability is indeed prevalent in our system, allowing for striking pairwise outcome changes that propagate up to multispecies communities. These results argue that a bottom-up approach can provide insight into how communities will change under stress.

ecology↗