Epigenetics and Evolutionary Processes (2015)

Josh Banta and Christina Richards (Department of Integrative Biology, University of South Florida) organized a symposium at the 2015 Evolution meetings in Guarujá, Brazil, entitled, "Epigenetics and Evolutionary Processes." The symposium was sponsored by the Society for the Study of Evolution.

(From left: Catarina Lira-Medeiros, Bob Schmitz, Josh Banta, Koen Verhoeven, Gil Smith, Liran Carmel, and Marta Robertson)

Synopsis. Scientists have abundant information on sequences for a variety of organisms, but have made little progress in understanding how the genome actually functions in creating complex traits that are adaptive in complex environments (Richards et al. 2009; Pigliucci 2010). One area that may contribute to this understanding is ecological and evolutionary epigenetics, which focuses the relationships between epigenetic variation and the axes of phenotypic variation that fuel evolutionary change. Epigenetic mechanisms can alter gene expression and organismal function without any alterations in DNA sequences (Richards 2006), leading to variation in diverse phenotypes (Cubas et al. 1999; Morgan et al. 1999; Rakyan et al. 2003; Manning et al. 2006; Kucharski et al. 2008; Cortijo et al. 2014). Furthermore, epigenetic modifications can vary among individuals and populations (Herrera and Bazaga 2010, 2011; Massicotte et al. 2011; Herrera et al. 2012; Liu et al. 2012; Massicotte and Angers 2012; Schrey et al. 2012). Epigenetic modifications can even be heritable (Jablonka and Raz 2009; Johannes et al. 2009; Verhoeven et al. 2010) and the phenotypic consequences of epigenetic changes have been observed in diverse taxa (animals: Gluckman et al. 2009; Snell-Rood et al. 2013; plants: Cubas et al. 1999; Bossdorf et al. 2010; Herrera and Bazaga 2011; Zhang et al 2013; fungi: Reyna-López et al. 1997; yeast: Herrera et al. 2012). Thus, epigenetic mechanisms are a potentially important mechanism of phenotypic change (Angers et al. 2010; Verhoeven et al. 2010; Richards et al. 2010; Cortijo et al. 2014). The study of epigenetic variation is already providing insights at both ecological and evolutionary time scales (Bossdorf et al. 2008; Richards et al. 2010; Latzel et al. 2013). Recent experimental screening for changes in methylation patterns has shown that epimutations can be induced by environmental stress, affect phenotype, and occur more rapidly than DNA sequence mutations (Johannes et al. 2009; Verhoeven et al. 2010; Cortijo et al. 2014). For this reason epigenetic effects could offer an alternative to genetic variation for rapid response to environmental challenges (Bossdorf et al. 2008), but so far few studies have begun to explore this possibility. While most of the work in ecological epigenetics to date has been done in plants, there are an increasing number of animal studies (Schrey et al 2013). This symposium highlights different approaches across systems that are making progress to understand the importance of epigenetics in evolutionary processes.

Rationale. Evolutionary biology is currently experiencing an emergence of several research areas beyond the scope of the Modern Synthesis, which merged Mendelian genetics with the study of evolution over 70 years ago (Huxley 1942). Epigenetics is one such research area of study. While epigenetics has been studied in a cellular/molecular/biomedical context for decades (Holliday 2006), it is now emerging as an active field of study in evolutionary biology, where it is being used to understand mechanisms of heritable phenotypic variation (Schrey et al. 2012). Yet because evolutionary epigenetics is still very young, it remains largely unexplored. We believe the time is ripe to start closing the gap between the number of molecular/cellular studies on epigenetics and the much smaller number of evolutionary studies on epigenetics.

Participants:

Dr. Joshua Banta, Assistant Professor, Department of Biology, University of Texas at Tyler.

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Understanding mechanisms of response to novel environments in invasive Japanese knotweed

Abstract. The expansion of invasive species provides an opportunity to investigate how organisms establish and adapt to new environments, but also challenges our understanding of the process of adaptation. Classic studies interested in adaptation have focused on DNA sequence variation, and the assumption that trait variation is based on sequence variation, but invasive species typically have low sequence based variation. There is now evidence to suggest that epigenetic effects can result in heritable, novel phenotypes even without variation in DNA sequence and could therefore provide an unappreciated source of response. We are exploring the potential role of epigenetic processes in invasive Japanese knotweed (Fallopia japonica) with a combination of classic ecological design and developing novel genomics techniques. These studies will enhance our understanding of how epigenetic variation may be shaped by environment and contribute to adaptation.

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Epigenome of tomato (Solanum lycopersicum) and its implications on the domestication process of this species

Abstract. Changes in DNA methylation of cytosines can be used as markers of biodiversity in wild species. The cytosine DNA methylation is an epigenetic phenomenon related to different processes such as genome stability and regulation of gene expression. Through the next-generation sequencing techniques, large scale epigenome studies have been carried out with model and wild plant species. Tomato is a species of great interest for agriculture and can be used in functional studies because of its wide range of genomic tools available. Moreover, little is known about the epigenetic process during its domestication. In order to elucidate about the epigenetic alterations resulted from the tomato domestication, we sequenced in Illumina bisulfite-treated libraries of two accessions of Solanum lycopersicum (domesticated tomato) and three accessions of S. pimpinellifolium (wild relative of tomato). All epigenomes were aligned with the reference genome of S. lycopersicum 2.50 from Solgenomics database using Bismark. Mapping efficiency was high for all libraries. Percentages of methylation in CpG, CHG and CHH context were similar to all libraries sequenced, 11%, 42%, 47%, respectivelly, showing proportionally less methylation in CpG regions. Also CpG methylation was not correlated to repeated regions nor centromeric regions. Preliminary comparative results show several genes with CpG regions differentially methylated between domesticated and wild tomato species (S. lycopersicum vs. S. pimpinellifolium). Further analysis are needed to comprehend the relation of differentially metylated CpG regions inside genes and promoters with differentially expressed genes within and between these two species of tomato and its accessions.

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Epigenetic inheritance in asexual plants: causes and consequences of heritable DNA methylation variation within apomictic dandelion lineages

Abstract. Heritable epigenetic modulation of gene expression is a candidate mechanism to explain parental environmental effects on offspring phenotypes, but current evidence for environment-induced epigenetic changes that persist in offspring generations is scarce. In apomictic dandelions, exposure to various stresses was previously shown to heritably alter DNA methylation patterns. In this study we explore whether these induced changes are accompanied by heritable effects on offspring phenotypes. We observed effects of parental jasmonic acid treatment on offspring specific leaf area and on offspring interaction with a generalist herbivore; and of parental nutrient stress on offspring root-shoot biomass ratio, tissue P-content and leaf morphology. Some of the effects appeared to enhance offspring ability to cope with the same stresses that their parents experienced. Effects differed between apomictic genotypes and were not always consistently observed between different experiments, especially in the case of parental nutrient stress. While this context-dependency of the effects remains to be further clarified, the total set of results provides evidence for the existence of transgenerational effects in apomictic dandelions. Zebularine treatment affected the within-generation response to nutrient stress, pointing at a role of DNA methylation in phenotypic plasticity to nutrient environments. This study shows that stress exposure in apomictic dandelions can cause transgenerational phenotypic effects, in addition to previously demonstrated transgenerational DNA methylation effects.

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Comparative epigenomics of DNA methylation within flowering plants

Abstract. Methylation of cytosines in plants is a prominent epigenomic feature and is involved in critical functions such as transposon silencing and regulating gene expression. We have compared the methylomes of >35 different plant species from across the angiosperms using whole genome bisulfite sequencing data. These results indicate widespread variance in the amount of CG, CHG, and CHH methylation across species which is indicative of the diversity of silencing pathways being used by plant genomes. Genes with CG gene-body methylation, associated stable gene expression and non-CG methylation, associated with silencing, were classified for each species. Molecular evolutionary analysis of CG gene-body genes shows that these genes are generally conserved in multiple features. Differences in the use of CHG and CHH methylation suggests that different methylation pathways may predominate in different species.

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Genome‐wide DNA methylation patterns in wild samples of two morphotypes of threespine stickleback (Gasterosteus aculeatus)

Abstract. Epigenetic marks such as DNA methylation play important biological roles in gene expression regulation and cellular differentiation during development. The role of epigenetic variation in evolution has been highly contested, yet information on naturally occurring epigenetic variation across species is lacking. To examine whether DNA methylation patterns are potentially associated with naturally occurring phenotypic differences, we examined genome-wide DNA methylation within G. aculeatus, using reduced representation bisulfite sequencing (RRBS). We sequenced the genomes of two stickleback phenotypes: complete lateral plate morphs (associated with marine populations) and low plate morphs (associated with freshwater populations). First, we identified highly methylated regions of the stickleback genome, determining the genomic locations of methylated regions and the genes associated with them. Next, we identified differentially methylated regions (DMRs) of the genome between complete and low lateral plate morphs, their genomic locations and associated genes.

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Paleo‐epigenetics: the DNA methylation maps of archaic humans

Abstract. A widely accepted evolutionary notion is that many phenotypic differences between closely related species may be attributed to changes in regulatory programs rather than to changes in protein sequence. Recent advances in ancient DNA sequencing yielded archaic human genomes at a quality that rivals that of present-day humans. This opens up an unprecedented opportunity to use genomic information in studying the recent evolution of gene regulation in humans. Here I present a novel method to reconstruct the complete DNA methylation map along ancient genomes, based on asymmetry between the deamination of methylated and unmethylated cytosines. I revealed ~2000 differentially methylated regions (DMRs) between archaic and present-day humans, and compiled a list of genes whose activity level had recently changed along our lineage. Examples include the HOXD9 and HOXD10 genes that may underlie the unique morphology of present-day humans. In general, these genes have high tendency to be associated with human diseases. This work comprises the first epigenetic map of an ancient genome, and provides the first insight to gene activity in archaic humans. Our method can be implicated on any future high-coverage ancient genome, and thus opens a window to a new field – paleo-epigenetics.

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Literature Cited

Angers B, Castonguay E, Massicotte R. 2010. Environmentally induced phenotypes and DNA methylation: how to deal with unpredictable conditions until the next generation and after. Mol Ecol 19:1283–95.

Bossdorf O, Richards CL, Pigliucci M. 2008. Epigenetics for ecologists. Ecol Lett 11:106–15.

Bossdorf O, Arcuri D, Richards CL, Pigliucci M. 2010. Experimental alteration of DNA methylation affects the phenotypic plasticity of ecologically relevant traits in Arabidopsis thaliana. Evol Ecol 24:541–53.

Cubas P, Vincent C, Coen E. 1999. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401:157–61.

Gluckman PD, Hanson MA, Buklijas T, Low FM, Beedle AS. 2009. Epigenetic mechanisms that underpin metabolic and cardiovascular diseases. Nat Rev Endocrinol 5:401–408.

Gokhman D, Lavi E, Prüfer K, Fraga MF, Riancho JA, Kelso J, Pääbo S, Meshorer E, Carmel L. 2014. Reconstructing the DNA methylation maps of the Neandertal and the Denisovan. Science 344: 523-527.

Herrera CM, Bazaga P. 2010. Epigenetic differentiation and relationship to adaptive genetic divergence in discrete populations of the violet Viola cazorlensis. New Phytol 187:867–76.

Herrera CM, Bazaga P. 2011. Untangling individual variation in natural populations: ecological, genetic and epigenetic correlates of long-term inequality in herbivory. Mol Ecol 20:1675–88.

Herrera CM, Pozo MI, Bazaga P. 2012. Jack of all nectars, master of most: DNA methylation and the epigenetic basis of niche width in a flower living yeast. Mol Ecol 21:2602–16.

Holliday R. 2006. Epigenetics: a historial overview. Epigenetics 1: 76-80.

Huxley J. 1942. Evolution: The Modern Synthesis. Allen & Unwin, London, UK.

Jablonka E, Raz G. 2009. Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q Rev Biol 84:131–76.

Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N, Bulski A, Albuisson J, Heredia F, Audigier P, et al. 2009. Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet 5:e1000530.

Kucharski R, Maleszka J, Foret S, Maleszka R. 2008. Nutritional control of reproductive status in honeybees via DNA methylation. Science 319:1827–30.

Latzel V., Allan E, Silveira AB, Colot V, Fischer M, Bossdorf O. 2013. Epigenetic diversity increases the productivity and stability of plant populations. Nat Comm 4: 2875.

Lira-Medeiros CF, Parisod C, Fernandes RA, Mata CS, Cardoso MA, Ferreira PCG. 2010. Epigenetic variation in mangrove plants occurring in contrasting natural environment. PLoS One 5:e10326.

Lu G, Xiaoming W, Biyun C, Guizhen G, Kun X. 2007. Evaluation of genetic and epigenetic modification in rapeseed (Brassica napus) induced by salt stress. J Integr Plant Biol 49:1599–607.

Manning K, Tor M, Poole M, Hong Y, Thompson AJ, King GJ, Giovannoni JJ, Seymour GB. 2006. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet 38:948–52.

Massicotte R, Whitelaw E, Angers B. 2011. DNA methylation: a source of random variation in natural populations. Epigenetics 6:421–7.

Massicotte R, Angers B. 2012. General-purpose genotype or how epigenetics extend the flexibility of a genotype. Gen Res Int 2012. Article ID 317175, 7 pp.

Pigliucci M. 2010. Genotype–phenotype mapping and the end of the ‘genes as blueprint’ metaphor. Philos Trans R Soc B 365:557–66.

Rakyan VK, Chong S, Champ ME, Cuthbert PC, Morgan HD, Luu KVK, Whitelaw E. 2003. Transgenerational inheritance of epigenetic states at the murine Axin (Fu) allele occurs after maternal and paternal transmission. Proc Natl Acad Sci U S A 100:2538–43.

Reyna-Lopez GE, Simpson J, Ruiz-Herrera J. 1997. Differences in DNA methylation patterns are detectable during the dimorphic transition of fungi by amplification of restriction polymorphisms. Mol Gen Genet 253:703–10.

Richards CL, Hanzawa Y, Ehrenreich IM, Katari M, Engelmann KE, Purugganan MD. 2009. Perspectives on ecological and evolutionary systems biology. In: Gutierrez RA, Coruzzi GM, editors. Plant systems biology. Annual Plant Reviews, Vol. 35. Oxford, UK: Blackwell Publishing. p. 331–51.

Richards CL, Bossdorf O, Verhoeven KJF. 2010. Understanding natural epigenetic variation. New Phytol 187:562–4.

Richards CL, Schrey A, Pigliucci M. 2012. Invasion of diverse habitats by few Japanese knotweed genotypes is correlated with epigenetic differentiation. Ecol Lett 15:1016–25.

Richards EJ. 2006. Inherited epigenetic variation—revisiting soft inheritance. Nat Rev Genet 7:395–401.

Schmitz RJ, Schultz MD, Lewsey MG, O’Malley RC, Urich MA, Libiger O, Schork NJ, Ecker RJ. 2011. Transgenerational epigenetic instability is a source of novel methylation variants. Science 334:369-373.

Schmitz RJ, Schultz MD, Urich MA, Nery JR, Pelizzola M, Libiger O, Alix A, McCosh RB, Chen H, Schork NJ, Ecker JR. 2013. Patterns of population epigenomic diversity. Nature 495: 193-198.

Schmitz RJ. 2014. The secret garden – epigenetic alleles underlie complex traits. Science 343:1082-1083.

Schrey A, Coon C, Grispo M, Awad M, McCoy E, Mushinsky H, Richards CL, Martin LB. 2012. Epigenetic variation may compensate for decreased genetic variation with introductions: a case study using house sparrows (Passer domesticus) on two continents. Genet Res Int 2012. Article ID 979751, 7 pp.

Schrey AW, Alvarez M, Foust C, Kilvitis HJ, Lee JD, Liebl AL, Martin LB, Richards CL, Robertson MH. 2013. Ecological Epigenetics: Beyond MS-AFLP. Int Comp Biol 53: 340-350.

Snell-Rood EC, Troth A, Moczek AP. 2013. DNA methylation as a mechanism of nutritional plasticity: Limited support from horned beetles. J. Exp Zool B Mol Dev Evol. 320: 22-34.

Smith G, Ritchie MG. 2013. How might epigenetics contribute to ecological speciation? Curr Zool 59: 686–696.

Suzuki MM, Bird A. 2008. DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genetics 9:465–76.

Verhoeven KJF, Jansen JJ, van Dijk PJ, Biere A. 2010. Stressinduced DNA methylation changes and their heritability in asexual dandelions. New Phytol 185:1108–18.

Zhang YY, Fischer M, Colot V, Bossdorf O. 2013. Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phyt 197: 314–322.