Genetics of local adaptation in Arabidopsis thaliana - seed dormancy as a case study

Local adaptation occurs when natural selection favours different phenotypes in different locations. Here, I studied the genetics of adaptation using local adaptation for seed dormancy in Arabidopsis thaliana as a model system. I asked, is there local adaptation for seed dormancy and what environmental factors drive it? What is the genetic basis of adaptation and what is the molecular nature of adaptive changes? To answer these questions I conducted a population genetic study, comparing neutral markers, candidate genes and traits. Some QTL-mapping experiments were also performed. The results obtained indicate that there is local adaptation in seed dormancy and this is mediated by the amount of precipitation received during the summer months. Local adaptation seems to occur at a regional geographic scale. Based on genetic mapping and studies, the large effect gene DOG1 is mainly responsible for adaptation, together with several other loci with minor effects. A population genetic study of DOG1 revealed that there is a signature of local selection on DOG1. Several functional alleles of DOG1 are segregating in natural populations. Mutations that increase or decrease dormancy seem to have occurred several times independently. This likely happens because of a low migration rate, new mutations occur in separate populations but they cannot migrate efficiently to other populations and thus no single mutation becomes fixed. The molecular basis of adaptive changes could not be determined, yet some candidate mutations for functional changes were identified. In addition, some of the results raised concerns about the proper way to estimate genetic differentiation. Therefore, the statistical properties of some estimators of genetic differentiation were studied using computer simulations. An estimator that takes mutation model into account can be used to compare different types of markers

Influence of mutation rate on estimators of genetic differentiation - lessons from Arabidopsis thaliana

It has been brought to our attention that our paper (Kronholm et al. BMC Genetics 2010, 11: 33) may have caused some confusion for readers interested in the correct quantification of population differentiation. We feel that this issue is of some importance and wish to clarify any confusion that might have resulted

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 amount of epigenetic variation available to populations can reduce adaptation in environments where it otherwise happens. From genomic and epigenomic sequences from a subset of the populations, we see changes in methylation patterns between the evolved populations over-represented in some functional categories of genes, which is consistent with some of these differences being adaptive. Based on whole genome sequencing of evolved clones, the majority of DNA methylation changes do not appear to be linked to cis-acting genetic mutations. Our results show that transgenerational epigenetic effects play a role in adaptive evolution, and suggest that the relationship between changes in methylation patterns and differences in evolutionary outcomes, at least for quantitative traits such as cell division rates, is complex

Prolonged sleep restriction induces changes in pathways involved in cholesterol metabolism and inflammatory responses

Sleep loss and insufficient sleep are risk factors for cardiometabolic diseases, but data on how insufficient sleep contributes to these diseases are scarce. These questions were addressed using two approaches: an experimental, partial sleep restriction study (14 cases and 7 control subjects) with objective verification of sleep amount, and two independent epidemiological cohorts (altogether 2739 individuals) with questions of sleep insufficiency. In both approaches, blood transcriptome and serum metabolome were analysed. Sleep loss decreased the expression of genes encoding cholesterol transporters and increased expression in pathways involved in inflammatory responses in both paradigms. Metabolomic analyses revealed lower circulating large HDL in the population cohorts among subjects reporting insufficient sleep, while circulating LDL decreased in the experimental sleep restriction study. These findings suggest that prolonged sleep deprivation modifies inflammatory and cholesterol pathways at the level of gene expression and serum lipoproteins, inducing changes toward potentially higher risk for cardiometabolic diseases.Peer reviewe

Evolution of anticipatory effects mediated by epigenetic changes

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 plasticity, bet-hedging, or by tracking the environment with genetic adaptation, in addition to the evolution of anticipatory effects. The results show that anticipatory effects evolve when the environmental cue provides reliable information about the environment and the environment changes at intermediate rates, provided that fitness costs of anticipatory effects are rather low. Moreover, evolution of anticipatory effects is quite robust to different genetic architectures when reliability of the environmental cue is high. Anticipatory effects always give smaller fitness benefits than within generation plasticity, suggesting a possible reason for generally small observed anticipatory effects in empirical studies.peerReviewe

Kronholm_data

Kronholm_dat

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 temperature, we tested the roles of different epigenetic mechanisms in response to fluctuating environments using different mutants. We found that growth of Neurospora can be predicted in fluctuating temperatures to some extent if acclimation times are taken into account in the model. Interestingly, while fluctuating environments have been linked with epigenetic responses we found only some evidence of involvement of epigenetic mechanisms on tolerating fluctuating temperatures. Mutants which lacked H3K4 or H3K36 methylation had slightly impaired response to temperature fluctuations, in addition the H3K4 methylation mutant and a mutant in the RNA interference pathway had altered acclimation times

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 evolved in constant and two fluctuating environments. We found that strains that evolved in fluctuating environments exhibited larger environmental variation suggesting that adaptation to fluctuations has decreased the visibility of genetic variation to selection.peerReviewe

Kronholm_Ketola_data_scripts

The data and R scripts required to repeat the analyses done in the manuscript. Contains a readme file with explanations for the different files and column names

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. The effect of epigenetic mutations on adaptive walks depends crucially on their stability and fitness effects relative to genetic mutations, with small-effect epigenetic mutations generally speeding adaptation, and epigenetic mutations with the same fitness effects as genetic mutations slowing adaptation. Our work reveals a complex relationship between epigenetic mutations and natural selection and highlights the need for empirical data