Search bioRxiv⌕ Search

Biology subjects

Otto, S. P.

Publications and source records attributed to Otto, S. P..

At least 19 recordsLinked to original sources

Evolutionary rescue in toxic combinations of metal is dependent on metal interactions

Populations facing abrupt environmental change may avoid extinction through evolutionary rescue, in which beneficial mutations allow individuals to survive and reproduce under otherwise lethal conditions. However, theory on evolutionary rescue has largely focused on single stressors, leaving open how interactions among simultaneous stressors shape adaptation. In particular, synergistic interactions, which amplify toxicity, and antagonistic interactions, which reduce it, may impose distinct selective pressures and lead to different fitness outcomes. To investigate this, we experimentally evolved Saccharomyces cerevisiae under lethal combinations of six metals (Cd, Co, Cu, Mn, Ni, and Zn), obtaining rescued lines in eight of the fifteen pairwise combinations. We then measured the fitness of evolved lines in the original metal combination, each component metal individually, and the ancestral environment. Adaptation differed systematically with metal interactions: lines evolved in antagonistic combinations generally gained fitness in the individual metals as well as in the combination, whereas lines evolved in synergistic combinations tended to show more specialized adaptation, with fitness benefits concentrated in the combination and reduced fitness in the component metals. No rescue was observed in combinations whose toxicity was consistent with concentration addition, although differences in the precise toxicity of experimental treatments may have influenced rescue outcomes. These findings demonstrate that interactions among simultaneous stressors can shape not only the likelihood of evolutionary rescue but also the breadth of its fitness benefits, highlighting the importance of accounting for stressor interactions when investigating evolutionary responses to environmental change.

evolutionary biology↗

Pleiotropy links host axes of defense against a pathogen

Organisms face ubiquitous threats from pathogens, and in response hosts have evolved a cascade of defenses to avoid, resist, or tolerate infection. While these stepwise defenses may act independently, they can be pleiotropically linked via shared molecular mechanisms, regulation, and crosstalk. Here, we tested the extent to which pleiotropy shapes multiple axes of defense using knockouts of 16 single genes involved in innate immunity of Caenorhabditis elegans against the opportunistic bacterial pathogen Pseudomonas aeruginosa. Host genotype had variable effects on components of host defense. Traits such as infection-induced mortality and body size varied frequently across host genotypes, while behavioral avoidance, bacterial uptake, and susceptibility to bacterial colonization varied less frequently. Broadly, pleiotropy between defenses was common, driving patterns of variation that linked several traits together. However, important components of defense like mortality, avoidance, and susceptibility to colonization were more independent from one another. Our results show that pleiotropy between defenses can be common, highlighting the importance of moving beyond single phenotypes to understand multiple dimensions of host-pathogen interactions.

immunology↗

Elevated mutation near crossovers inhibits the evolution of recombination

Recombination diversifies offspring genomes and helps ensure chromosome segregation during meiosis. Mutation rates are elevated near crossovers due to the induction of double-strand breaks and their imperfect repair, a byproduct of recombination typically ignored by theory designed to explain its evolution. To examine the evolutionary role of recombination-associated mutation, we analyze a population genetic model in which a modifier locus controls both the rate of recombination between two loci experiencing viability selection and the rate of mutation at those loci. Analytical and numerical results demonstrate that the advantage of recombination conferred by its capacity to remove epistatic, deleterious mutations is overcome by the selective cost of even small increases in the mutation rate. Simulations of finite populations show that recombination-associated mutation also decreases the probability of fixation of modifier alleles in the absence of epistasis. By incorporating the mutagenic effects of recombination, our analysis extends a rich body of theory to incorporate a molecular feature inherent in the formation of crossovers. Our findings suggest that higher recombination rate evolves by altering steps in the crossover pathway that are less likely to inflict mutational damage.

evolutionary biology↗

Tip rate estimates can predict future diversification, but are unreliable and context dependent

Understanding the variability of processes leading to the emergence of new lineages is one of the major tasks of macroevolution as a scientific field. Recent years have seen the rise of rate-variable diversification models and metrics that estimate the rates of species diversification at the tips of phylogenetic trees and are thus potentially useful for predicting future evolutionary success of individual species. These methods use various assumptions about the variability and heritability of diversification rates. However, the general performance of rate-variable diversification methods have never been consistently tested against real world data. Here we explore the capacity of multiple rate-variable diversification methods to predict near-future diversification using temporal slices of empirical fossil and extant phylogenies. We do this using a newly developed approach similar to generalized linear models, allowing us to quantify the relationship between predictor tip rates and subsequent diversification rates derived from a probability distribution of numbers of daughter species. We find that tip rates estimated from current methods have non-zero but limited capacity to predict diversification in both fossil and extant phylogenies. The quality of the predictions depends not only on the methods used but also on the specific phylogeny, suggesting that diversification dynamics in some taxa may be more predictable in principle. Our results suggest that future cladogenesis can be, to a certain extent, predicted using existing tip rate methods, but the quality of such predictions is highly variable and depends on factors that are difficult to evaluate in practical applications.

evolutionary biology↗

Quantifying the effect of metal interactions on growth rate in Saccharomyces cerevisiae

Environmental stressors often co-occur, yet their combined effects on organisms remain poorly understood. As multifactorial anthropogenic changes intensify and alter environmental selection pressures, our understanding of stressor interactions is becoming increasingly important. However, established methods for characterizing the effects of stressor interactions can involve considerable experimental and computational labour. Here, we investigate how pairwise combinations of six divalent metal ions (Cd2+, Co2+, Cu2+, Mn2+, Ni2+, and Zn2+) affect the growth of Saccharomyces cerevisiae, using a high-throughput assay to generate concentration-response surfaces for all 15 combinations. We introduce{delta} , an easily calculable metric that quantifies the toxicity of a mixture relative to the toxicities of its individual components, and compare it to an established metric for synergism/antagonism, a, determined by calculating deviation from a null model of additivity, i.e., "concentration addition". Yeast growth rates reveal that metal mixture toxicity varies widely from the additive expectation with the effect of the combination ranging from greatly enhanced toxicity to greatly attenuated toxicity. Combinations with copper were more toxic than expected, and combinations with manganese or nickel were less. These trends correspond to known redox activities and metal-binding properties, pointing to possible mechanistic underpinnings rooted in oxidative stress and metal cofactor displacement. Furthermore, we find that a correlates with overlap in known metal resistance genes and similarity in redox potential, offering predictive insight into effects of metal interactions. While a provides a model-based measure of synergism or antagonism,{delta} serves as an intuitive, concentration-robust descriptor of ecological impact. Together, these metrics highlight the complexity of metal-metal interactions and the importance of accounting for nonadditive effects in ecotoxicological assessments. This framework provides a basis for evaluating mixture toxicity across diverse taxa and stressor types, with implications for both evolutionary biology and environmental risk assessment.

ecology↗

Variety is the spice of life: nongenetic variation in life histories influences population growth and evolvability

Individual vital rates are key determinants of lifetime reproductive success, and variability in these rates shapes population dynamics. Previous studies have found that this vital rate hetero-geneity can influence demographic properties including population growth rates, however, the explicit effects of the amount of variation within and the covariance between vital rates that can also vary throughout the lifespan on population growth remains unknown. Here, we explore the analytical consequences of nongenetic heterogeneity on long-term population growth rates and rates of evolution by modifying traditional age-structured population projection matrices to incorporate variation among individual vital rates. The model allows vital rates to be permanent throughout life ("fixed condition") or to change over the lifespan ("dynamic condition"). We reduce the complexity associated with adding individual heterogeneity to age-structured models through a novel application of matrix collapsing ("phenotypic collapsing"), showing how to collapse in a manner that preserves the asymptotic and transient dynamics of the original matrix. The main conclusion is that nongenetic individual heterogeneity can strongly impact the longterm growth rate and rates of evolution. The magnitude and sign of this impact depends heavily on how the heterogeneity covaries across the lifespan of an organism. Our results emphasize that nongenetic variation cannot simply be viewed as random noise, but rather that it has consistent, predictable effects on fitness and evolvability.

evolutionary biology↗

The Prokaryotic and Eukaryotic Microbiome of Pacific Oyster Spat is Shaped by Ocean Warming but not Acidification

Pacific oysters (Magallana gigas, also known as Crassostrea gigas), the most widely farmed oysters, are under threat from climate change and emerging pathogens. In part, their resilience may be affected by their microbiome, which, in turn, may be influenced by ocean warming and acidification. Consequently, for three weeks, we exposed early-development Pacific oyster spat to different temperatures (18 and 24 {degrees}C) and pCO2 levels (800, 1600 and 2800 {micro}atm) in a fully crossed design. Under all conditions, the microbiome developed over time, with potentially pathogenic ciliates (Uronema marinum) greatly reduced in all treatments, suggesting that the spats microbiome undergoes adaptive shifts as the oysters age. The microbiome composition also differed significantly with temperature, but not acidification, indicating that M. gigas spat microbiomes can be altered by ocean warming but resilient to ocean acidification in our experiments. These findings highlight the spat microbiomes flexibility to environmental changes as well as its "protective" capability against potentially pathogenic microbes.

microbiology↗

Density-dependent selection during range expansion affects expansion load in life-history traits

Models of range expansion have independently explored fitness consequences of life-history trait evolution and increased rates of genetic drift--or "allele surfing"--during spatial spread, but no previous model has examined the interactions between these two processes. Here, we explore an ecologically complex range expansion scenario that combines density-dependent selection with allele surfing, using spatially explicit simulations to asses the genetic and fitness consequences of density-dependent selection on the evolution of life-history traits. We demonstrate that density-dependent selection on the range edge acts differently depending on the life-history trait and can either diminish or enhance allele surfing. Specifically, we show that selection on the range edge is always weaker at sites affecting competitive ability (K-selected traits) than intrinsic growth rate ((r-selected traits). We then link differences in the frequency of deleterious mutations to differences in the efficacy of selection and rate of mutation accumulation across distinct life-history traits. Finally, we demonstrate the fitness consequences of accumulated deleterious mutations for different life-history traits are related to the population density in which they are expressed. Our work highlights the complex relationship between ecology and expressed genetic load, which will be important to consider when interpreting both experimental and field studies of range expansion.

evolutionary biology↗

Trait-dependent diversification in angiosperms: patterns, models and data

Variation in species richness across the tree of life, accompanied by the incredible variety of ecological and morphological characteristics found in nature, has inspired many studies to link traits with species diversification. Angiosperms are a highly diverse group that has fundamentally shaped life on earth since the Cretaceous, and illustrate how species diversification affects ecosystem functioning. Numerous traits and processes have been linked to differences in species richness within this group, but we know little about how these interact and their relative importance. Here, we synthesized data from 152 studies that used state-dependent speciation and extinction (SSE) models on angiosperm clades. Intrinsic traits related to reproduction and morphology were often linked to diversification but a set of universal drivers did not emerge as traits did not have consistent effects across clades. Importantly, dataset properties were correlated to SSE model results - trees that were larger, older, or less well-sampled tended to yield trait-dependent outcomes. We compared these properties to recommendations for SSE model use and provide a set of best practices to follow when designing studies and reporting results. Finally, we argue that SSE model inferences should be considered in a larger context incorporating species ecology, demography and genetics.

evolutionary biology↗

Rapid adaptation and range expansion in response to agriculture over the last two centuries

North America has seen a massive increase in cropland use since 1800, accompanied more recently by the intensification of agricultural practices. Through genome analysis of present-day and historical samples spanning environments over the last two centuries, we studied the impact of these changes in farming on the extent and tempo of evolution across the native range of common waterhemp (Amaranthus tuberculatus), a now pervasive agricultural weed. Modern agriculture has imposed strengths of selection rarely observed in the wild, with striking shifts in allele frequency trajectories since agricultural intensification in the 1960s. An evolutionary response to this extreme selection was facilitated by a concurrent human-mediated range shift. By reshaping genome-wide diversity across the landscape, agriculture has driven the success of this weed in the 21st-century. One Sentence SummaryModern agriculture has shaped the evolution of a native plant into a weed by driving range shifts and strengths of selection rarely observed in the wild.

evolutionary biology↗

Broad variation in rates of polyploidy and dysploidy across flowering plants is correlated with lineage diversification

Changes in chromosome number are considered an important driver of diversification in angiosperms. Single chromosome number changes caused by dysploidy may produce strong reproductive barriers leading to speciation. Polyploidy, or whole genome duplication, yields new species that are often reproductively isolated from progenitors and may exhibit novel morphology or ecology that may further facilitate diversification. Here, we examined the rates of polyploidy, dysploidy, and diversification across the angiosperms. Our analyses of nearly 30,000 taxa representing 46 orders and 147 families found that rates of polyploidy and dysploidy differed by two to three orders of magnitude. The rates of polyploidy and dysploidy were positively correlated with diversification rates, but relative importance analyses indicated that variation in polyploidy was better correlated with diversification rates than dysploidy. Our results provide an overview of angiosperm chromosomal evolution and a roadmap for future research on the complex relationships among polyploidy, dysploidy, and diversification.

evolutionary biology↗

Fixation and effective size in a haploid-diploid population with asexual reproduction

The majority of population genetic theory assumes fully haploid or diploid organisms with obligate sexuality, despite complex life cycles with alternating generations being commonly observed. To reveal how natural selection and genetic drift shape the evolution of haploid-diploid populations, we analyze a stochastic genetic model for populations that consist of a mixture of haploid and diploid individuals, allowing for asexual reproduction and niche separation between haploid and diploid stages. Applying a diffusion approximation, we derive the fixation probability and describe its dependence on the reproductive values of haploid and diploid stages, which depend strongly on the extent of asexual reproduction in each phase and on the ecological differences between them. Highlight- Classical models consider fully haploid or diploid populations - We model haploid-diploid life cycles allowing for asexual reproduction - We obtain the fixation probability of alleles subject to selection and drift - Reproductive values of haploid and diploid stages shape their evolution

genetics↗

Feedback Between Coevolution and Epidemiology Can Help or Hinder the Maintenance of Genetic Variation in Host-Parasite Models

Understanding if and when coevolution helps maintains genetic variation in hosts of a directly-transmissible pathogen is fundamental to quantifying the prevalence and impact of coevolution on disease epidemiology. Here, we extend our previous work on the maintenance of genetic variation in a classic matching-alleles coevolutionary model by exploring the effects of ecological and epidemiological feedbacks, where both allele frequencies and population sizes are allowed to vary over time. In general, we find that coevolution rarely maintains more host genetic variation than expected under neutral genetic drift alone. When and if coevolution maintains or depletes genetic variation relative to neutral drift is determined, predominantly, by two factors: the deterministic stability of the Red Queen allele frequency cycles and the frequency at which pathogen fixation occurs, as this results in directional selection and the depletion of genetic variation in the host. Compared to purely coevolutionary models with constant host and pathogen population sizes, ecological and epidemiological feedbacks stabilize Red Queen cycles deterministically, but population fluctuations in the pathogen increase the rate of pathogen fixation, especially in epidemiological models. Taken together our results illustrate the importance of considering the ecological and epidemiological context in which coevolution occurs when examining the impact of Red Queen cycles on genetic variation.

evolutionary biology↗

Coevolution does not slow the rate of loss of heterozygosity in a stochastic host-parasite model with constant population size

Coevolutionary negative frequency dependent selection has been hypothesized to maintain genetic variation in host and parasites. Despite the extensive literature pertaining to host-parasite coevolution, the effect of matching-alleles (MAM) coevolution on the maintenance of genetic variation has not been explicitly modelled in a finite population. The dynamics of the MAM in an infinite population, in fact, suggests that genetic variation in these coevolving populations behaves neutrally. We find that while this is largely true in finite populations two additional phenomena arise. The first of these effects is that of coevolutionary natural selection on stochastic perturbations in host and pathogen allele frequencies. While this may increase or decrease genetic variation, depending on the parameter conditions, the net effect is small relative to that of the second phenomena. Following fixation in the pathogen, the MAM becomes one of directional selection, which in turn rapidly erodes genetic variation in the host. Hence, rather than maintain it, we find that, on average, matching-alleles coevolution depletes genetic variation.

evolutionary biology↗

Evolution of plasticity in production and transgenerational inheritance of small RNAs under dynamic environmental conditions

In a changing environment, small RNAs (sRNAs) play an important role in the post-transcriptional regulation of gene expression and can vary in abundance depending on the conditions experienced by an individual (phenotypic plasticity) and its parents (non-genetic inheritance). Many sRNAs are unusual in that they can be produced in two ways, either using genomic DNA as the template (primary sRNAs) or existing sRNAs as the template (secondary sRNAs). Thus, organisms can evolve rapid plastic responses to their current environment by adjusting the amplification rate of sRNA templates. sRNA levels can also be transmitted transgenerationally by the direct transfer of either sRNAs or the proteins involved in amplification. Theory is needed to describe the selective forces acting on sRNA levels, accounting for the dual nature of sRNAs as regulatory elements and templates for amplification and for the potential to transmit sRNAs and their amplification agents to offspring. Here, we develop a model to study the dynamics of sRNA production and inheritance in a fluctuating environment. We tested the selective advantage of mutants capable of sRNA-mediated phenotypic plasticity within resident populations with fixed levels of sRNA transcription. Even when the resident was allowed to evolve an optimal constant rate of sRNA production, plastic amplification rates capable of responding to environmental conditions were favored. By contrast, mechanisms allowing sRNA transcripts or amplification agents to be inherited were favored primarily when parents and offspring face similar environments and when selection acts before the optimal level of sRNA can be reached within the organism. Our study provides a clear set of testable predictions for the evolution of sRNA-related mechanisms of phenotypic plasticity and transgenerational inheritance.

evolutionary biology↗

Genetic paths to evolutionary rescue and the distribution of fitness effects along them

The past century has seen substantial theoretical and empirical progress on the genetic basis of adaptation. Over this same period a pressing need to prevent the evolution of drug resistance has uncovered much about the potential genetic basis of persistence in declining populations. However, we have little theory to predict and generalize how persistence - by sufficiently rapid adaptation - might be realized in this explicitly demographic scenario. Here we use Fishers geometric model with absolute fitness to begin a line of theoretical inquiry into the genetic basis of evolutionary rescue, focusing here on asexual populations that adapt through de novo mutations. We show how the dominant genetic path to rescue switches from a single mutation to multiple as mutation rates and the severity of the environmental change increase. In multi-step rescue, intermediate genotypes that themselves go extinct provide a springboard to rescue genotypes. Comparing to a scenario where persistence is assured, our approach allows us to quantify how a race between evolution and extinction leads to a genetic basis of adaptation that is composed of fewer loci of larger effect. We hope this work brings awareness to the impact of demography on the genetic basis of adaptation.

evolutionary biology↗

Insights from Fisher’s geometric model on the likelihood of speciation under different histories of environmental change

The formation of new species via the accumulation of incompatible genetic changes is thought to result either from ecologically-based divergent natural selection or the order by which mutations happen to arise, leading to different evolutionary trajectories even under similar selection pressures. There is growing evidence in support of both ecological speciation and mutation-order speciation, but how different environmental scenarios affect the rate of species formation remains underexplored. We use a simple model of optimizing selection on multiple traits ("Fishers geometric model") to determine the conditions that generate genetic incompatibilities in a changing environment. We find that incompatibilities are likely to accumulate in isolated populations adapting to different environments, consistent with ecological speciation. Incompatibilities also arise when isolated populations face a similar novel environment; these cases of mutation-order speciation are particularly likely when the environment changes rapidly and favors the accumulation of large-effect mutations. In addition, we find that homoploid hybrid speciation is likely to occur either when new environments arise in between the parental environments or when parental populations have accumulated large-effect mutations following a period of rapid adaptation. Our results indicate that periods of rapid environmental change are particularly conducive to speciation, especially mutation-order or hybrid speciation.

evolutionary biology↗

Haploid selection, sex ratio bias, and transitions between sex-determining systems

Sex determination is remarkably dynamic; many taxa display shifts in the location of sex-determining loci or the evolution of entirely new sex-determining systems. Predominant theories for why we observe such transitions generally conclude that novel sex-determining systems are favoured by selection if they equalise the sex ratio or increase linkage with a locus that experiences different selection in males vs. females. We use population genetic models to extend these theories in two ways: (1) We consider the dynamics of loci very tightly linked to the ancestral sex-determining loci, e.g., within the non-recombining region of the ancestral sex chromosomes. Variation at such loci can favour the spread of new sex-determining systems in which the heterogametic sex changes (XY to ZW or ZW to XY) and the new sex-determining region is less closely linked (or even unlinked) to the locus under selection. (2) We consider selection upon haploid genotypes either during gametic competition (e.g., pollen competition) or meiosis (i.e., non-Mendelian segregation), which can cause the zygotic sex ratio to become biased. Haploid selection can drive transitions between sex-determining systems without requiring selection to act differently in diploid males vs. females. With haploid selection, we find that transitions between male and female heterogamety can evolve where linkage with the sex-determining locus is either strengthened or weakened. Furthermore, we find that sex-ratio biases may increase or decrease with the spread of new sex chromosomes, which implies that transitions between sex-determining systems cannot be simply predicted by selection to equalise the sex ratio. In fact, under many conditions, we find that transitions in sex determination are favoured equally strongly in cases where the sex ratio bias increases or decreases. Overall, our models predict that sex determination systems should be highly dynamic, particularly when haploid selection is present, consistent with the evolutionary lability of this trait in many taxa.\n\nAuthor summarySystems of sex determination are strikingly diverse and labile in many clades. This poses the question: what drives transitions between sex-determining systems? Here, we use models to derive conditions under which new sex-determining systems spread. Prevailing views suggest that new sex-determining systems are favoured when they equalize the sex ratio and/or when they are more closely linked to genes that experience differential selection in males and females. Our models include selection upon haploid genotypes (meiotic drive or gametic competition), which biases the sex-ratio and occurs differently in male and female gametes. Surprisingly, we find the two forces (selection to equalize the sex ratio and the benefits of hitchhiking alongside driven alleles that distort the sex ratio) will often be equally strong, and thus neither is sufficient to explain the spread of new sex-determining systems in every case. We also find that new sex-determining alleles can spread despite being less closely linked to selected loci as long as initial linkage is tight or haploid selection is present. Our models therefore predict that loci in previously unexpected genomic locations and/or experiencing various types of selection (including haploid selection) can now be implicated as drivers of transitions between sex-determining systems.

evolutionary biology↗