Environmentally triggered evolutionary cascade across trophic levels in an experimental phage-bacteria-insect system
Abstract Environmental changes can cause strong cascading effects in species communities due to altered biological interactions between species (Zarnetske et al., 2012). Highly specialized interactions arising from the co-evolution of hosts and parasites, such as bacteria and phages, and short generation times of these species could rapidly lead to considerable evolutionary changes in their biotic interactions (Kerr, 2012; Buck and Ripple, 2017), with potential large-scale ramifications to other trophic levels. Here we report experimental evidence of cascading environmental effects across trophic levels in an experimental system where phage-bacteria coevolution in an abiotically altered env…
Effects of acclimation time and epigenetic mechanisms on growth of Neurospora in fluctuating environments
AbstractReaction norms or tolerance curves have often been used to predict how organisms deal with fluctuating environments. A potential drawback is that reaction norms measured in different constant environments may not capture all aspects of organismal responses to fluctuating environments. We examined growth of the filamentous fungusNeurospora crassain fluctuating temperatures and tested if growth in fluctuating temperatures can be explained simply by growth in different constant temperatures or if more complex models are needed. In addition, as previous studies on fluctuating environments have revealed that past temperatures that organisms have experienced can affect their response to c…
Epigenetic mutations can both help and hinder adaptive evolution.
Epigenetic variation is being integrated into our understanding of adaptation, yet we lack models on how epigenetic mutations affect evolution that includes de novo genetic change. We model the effects of epigenetic mutations on the dynamics and endpoints of adaptive walks—a process where a series of beneficial mutations move a population towards a fitness optimum. We use an individual-based model of an asexual population, where mutational effects are drawn from Fisher's geometric model. We find cases where epigenetic mutations speed adaptation or result in populations with higher fitness. However, we also find cases where they slow adaptation or result in populations with lower fitness. Th…
Crowdsourced analysis of fungal growth and branching on microfluidic platforms
Fungal hyphal growth and branching are essential traits that allow fungi to spread and proliferate in many environments. This sustained growth is essential for a myriad of applications in health, agriculture, and industry. However, comparisons between different fungi are difficult in the absence of standardized metrics. Here, we used a microfluidic device featuring four different maze patterns to compare the growth velocity and branching frequency of fourteen filamentous fungi. These measurements result from the collective work of several labs in the form of a competition named the “Fungus Olympics.” The competing fungi included five ascomycete species (ten strains total), two basidiomycete…
Chromatin structure influences rate and spectrum of spontaneous mutations in Neurospora crassa
While mutation rates have been extensively studied, variation in mutation rates throughout the genome is poorly understood. To understand patterns of genetic variation, it is important to understand how mutation rates vary. Chromatin modifications may be an important factor in determining variation in mutation rates in eukaryotic genomes. To study variation in mutation rates, we performed a mutation accumulation experiment in the filamentous fungus Neurospora crassa, and sequenced the genomes of the 40 MA lines that had been propagated asexually for approximately 1015 [1003, 1026] mitoses. We detected 1322 mutations in total, and observed that the mutation rate was higher in regions of low …
The effect of a temperature-sensitive prophage on the evolution of virulence in an opportunistic bacterial pathogen
AbstractViruses are key actors of ecosystems and have major impacts on global biogeochemical cycles. Prophages deserve particular attention as they are ubiquitous in bacterial genomes and can enter a lytic cycle when triggered by environmental conditions. We explored how temperature affects the interactions between prophages and other biological levels by using an opportunistic pathogen, the bacterium Serratia marcescens, that harbours several prophages and that had undergone an evolution experiment under several temperature regimes. We found that the release of one of the prophages was temperature-sensitive and malleable to evolutionary changes. We further discovered that the virulence of …
Adaptive Evolution and Epigenetics
Epigenetic changes, such as DNA methylation and certain histone modifications, can be inherited but in many cases they do not follow Mendelian inheritance patterns and their stability appears to be lower than for changes in DNA sequence. Adaptive evolution by natural selection requires that differences among individuals are heritable to some degree. Epigenetic changes can be incorporated into evolutionary theory, and given that properties of epigenetic variation are distinct from genetic variation, spontaneous epigenetic changes can affect evolutionary dynamics in interesting ways. In this chapter, I review the properties of epigenetic variation and how they relate to the main parameters of…
Parental effects in a filamentous fungus : Phenotype, fitness and mechanism
AbstractAdaptation to changing environments often requires meaningful phenotypic modifications to match the current conditions. However, obtaining information about the surroundings during an organism’s own lifetime may only permit accommodating relatively late developmental modifications. Therefore, it may be advantageous to rely on inter-generational or trans-generational cues that provide information about the environment as early as possible to allow development along an optimal trajectory. Transfer of information or resources across generations, known as parental effects, is well documented in animals and plants but not in other eukaryotes, such as fungi. Understanding parental effects…
Ecological plant epigenetics: Evidence from model and non-model species, and the way forward
Growing evidence shows that epigenetic mechanisms contribute to complex traits, with implications across many fields of biology. In plant ecology, recent studies have attempted to merge ecological experiments with epigenetic analyses to elucidate the contribution of epigenetics to plant phenotypes, stress responses, adaptation to habitat, and range distributions. While there has been some progress in revealing the role of epigenetics in ecological processes, studies with non-model species have so far been limited to describing broad patterns based on anonymous markers of DNA methylation. In contrast, studies with model species have benefited from powerful genomic resources, which contribute…
Quantitative genetics of temperature performance curves of Neurospora crassa
AbstractEarth’s temperature is increasing due to anthropogenic CO2emissions; and organisms need either to adapt to higher temperatures, migrate into colder areas, or face extinction. Temperature affects nearly all aspects of an organism’s physiology via its influence on metabolic rate and protein structure, therefore genetic adaptation to increased temperature may be much harder to achieve compared to other abiotic stresses. There is still much to be learned about the evolutionary potential for adaptation to higher temperatures, therefore we studied the quantitative genetics of growth rates in different temperatures that make up the thermal performance curve of the fungal model systemNeuros…
Evolutionary rescue at different rates of environmental change is affected by trade-offs between short-term performance and long-term survival.
As climate change accelerates and habitats free from anthropogenic impacts diminish, populations are forced to migrate or to adapt quickly. Evolutionary rescue (ER) is a phenomenon, in which a population is able to avoid extinction through adaptation. ER is considered to be more likely at slower rates of environmental change. However, the effects of correlated characters on evolutionary rescue are seldom explored yet correlated characters could play a major role in ER. We tested how evolutionary background in different fluctuating environments and the rate of environmental change affect the probability of ER by exposing populations of the bacteria Serratia marcescens to two different rates …
Experimental evolution of evolutionary potential in fluctuating environments
Variation is the raw material for evolution. Evolutionary potential is determined by the amount of genetic variation, but evolution can also alter the visibility of genetic variation to natural selection. Fluctuating environments are suggested to maintain genetic variation but they can also affect environmental variance, and thus, the visibility of genetic variation to natural selection. However, experimental studies testing these ideas are relatively scarce. In order to determine differences in evolutionary potential we quantified variance attributable to population, genotype and environment for populations of the bacterium Serratia marcescens. These populations had been experimentally evo…
Evolution of anticipatory effects mediated by epigenetic changes.
Abstract Anticipatory effects mediated by epigenetic changes occur when parents modify the phenotype of their offspring by making epigenetic changes in their gametes guided by information from an environmental cue. To investigate when do anticipatory effects mediated by epigenetic changes evolve in a fluctuating environment, I use an individual based simulation model with explicit genetic architecture. The model allows for the population to respond to environmental changes by evolving within generation plasticity, bet-hedging, or track the environment with genetic adaptation, in addition to the evolution of anticipatory effects. The results show that anticipatory effects evolve when the env…
Marked Neurospora crassa strains for competition experiments and Bayesian methods for fitness estimates
AbstractThe filamentous fungusNeurospora crassa, a model microbial eukaryote, has a life cycle with many features that make it suitable for studying experimental evolution. However, it has lacked a general tool for estimating relative fitness of different strains in competition experiments. To remedy this need, we constructedN. crassastrains that contain a modifiedcsr-1locus and developed an assay for detecting the proportion of the marked strain using a post PCR high resolution melting assay. DNA extraction from spore samples can be performed on 96-well plates, followed by a PCR step, which allows many samples to be processed with ease. Furthermore, we suggest a Bayesian approach for estim…
Adaptation to environmental stress at different timescales
Environments are changing rapidly, and to cope with these changes, organisms have to adapt. Adaptation can take many shapes and occur at different speeds, depending on the type of response, the trait, the population, and the environmental conditions. The biodiversity crisis that we are currently facing illustrates that numerous species and populations are not capable of adapting with sufficient speed to ongoing environmental changes. Here, we discuss current knowledge on the ability of animals and plants to adapt to environmental stress on different timescales, mainly focusing on thermal stress and ectotherms. We discuss within-generation responses that can be fast and induced within minute…
The effect of a temperature-sensitive prophage on the evolution of virulence in an opportunistic bacterial pathogen.
https://doi.org/10.1111/mec.16638 Abstract Viruses are key actors of ecosystems and have major impacts on global biogeochemical cycles. Prophages deserve particular attention as they are ubiquitous in bacterial genomes and can enter a lytic cycle when triggered by environmental conditions. We explored how temperature affects the interactions between prophages and other biological levels by using an opportunistic pathogen, the bacterium Serratia marcescens, that harbours several prophages and that had undergone an evolution experiment under several temperature regimes. We found that the release of one of the prophages was temperature-sensitive and malleable to evolutionary changes. We furthe…
Epigenetic control of phenotypic plasticity in a filamentous fungus Neurospora crassa
AbstractPhenotypic plasticity is the ability of a genotype to produce different phenotypes under different environmental or developmental conditions. Phenotypic plasticity is an ubiquitous feature of living organisms, and is typically based on variable patterns of gene expression. However, the mechanisms by which gene expression is influenced and regulated during plastic responses are poorly understood in most organisms. While modifications to DNA and histone proteins have been implicated as likely candidates for generating and regulating phenotypic plasticity, specific details of each modification and its mode of operation have remained largely unknown. In this study, we investigated how e…
Epigenetic Control of Phenotypic Plasticity in the Filamentous Fungus Neurospora crassa
Abstract Phenotypic plasticity is the ability of a genotype to produce different phenotypes under different environmental or developmental conditions. Phenotypic plasticity is a ubiquitous feature of living organisms, and is typically based on variable patterns of gene expression. However, the mechanisms by which gene expression is influenced and regulated during plastic responses are poorly understood in most organisms. While modifications to DNA and histone proteins have been implicated as likely candidates for generating and regulating phenotypic plasticity, specific details of each modification and its mode of operation have remained largely unknown. In this study, we investigated how e…
Roles of adenosine and cytosine methylation changes and genetic mutations in adaptation to different temperatures
Abstract Epigenetic modifications have been found to be involved in evolution, but the relative contributions of genetic and epigenetic variation in adaptation are unknown. Furthermore, previous studies on the role of epigenetic changes in adaptation have nearly exclusively focused on cytosine methylation in eukaryotes. We collected phenotypic, genetic, and epigenetic data from populations of the bacterium Serratia marcescens that had undergone experimental evolution in contrasting temperatures to investigate the relationship between environment, genetics, epigenetic, and phenotypic traits. The genomic distribution of methylated adenosines (m6A) pointed to their role in regulation of gene e…
Epigenetic and Genetic Contributions to Adaptation in Chlamydomonas
Epigenetic modifications, such as DNA methylation or histone modifications, can be transmitted between cellular or organismal generations. However, there are no experiments measuring their role in adaptation, so here we use experimental evolution to investigate how epigenetic variation can contribute to adaptation. We manipulated DNA methylation and histone acetylation in the unicellular green alga Chlamydomonas reinhardtii both genetically and chemically to change the amount of epigenetic variation generated or transmitted in adapting populations in three different environments (salt stress, phosphate starvation, and high CO2) for two hundred asexual generations. We find that reducing the …
Roles of adenine methylation and genetic mutations in adaptation to different temperatures in Serratia marcescens
AbstractEpigenetic modifications can contribute to adaptation, but the relative contributions of genetic and epigenetic variation are unknown. Previous studies on the role of epigenetic changes in adaptation in eukaryotes have nearly exclusively focused on cytosine methylation (m5C), while prokaryotes exhibit a richer system of methyltransferases targetting adenines (m6A) or cytosines (m4C, m5C). DNA methylation in prokaryotes has many roles, but its potential role in adaptation still needs further investigation. We collected phenotypic, genetic, and epigenetic data using single molecule real-time sequencing of clones of the bacterium Serratia marcescens that had undergone experimental evol…
Data from: Epigenetic mutations can both help and hinder adaptive evolution
Epigenetic variation is being integrated into our understanding of adaptation, yet we lack models on how epigenetic mutations affect evolution that includes de novo genetic change. We model the effects of epigenetic mutations on the dynamics and endpoints of adaptive walks-a process where a series of beneficial mutations move a population towards a fitness optimum. We use an individual-based model of an asexual population, where mutational effects are drawn from Fisher's geometric model. We find cases where epigenetic mutations speed adaptation or result in populations with higher fitness. However, we also find cases where they slow adaptation or result in populations with lower fitness. Th…
Data from: Effects of acclimation time and epigenetic mechanisms on growth of Neurospora in fluctuating environments
Reaction norms or tolerance curves have often been used to predict how organisms deal with fluctuating environments. A potential drawback is that reaction norms measured in different constant environments may not capture all aspects of organismal responses to fluctuating environments. We examined growth of the filamentous fungus Neurospora crassa in fluctuating temperatures and tested if growth in fluctuating temperatures can be explained simply by growth in different constant temperatures or if more complex models are needed. In addition, as previous studies on fluctuating environments have revealed that past temperatures that organisms have experienced can affect their response to current…
Supplemental Material for Kronholm et al., 2020
Supplementary material that includes a figure and table for article: Marked Neurospora crassa strains for competition experiments and Bayesian methods for fitness estimates. By Kronholm et al.