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Epigenetic variation among natural populations of the South African sandhopper Talorchestia capensis

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Abstract

Ecological epigenetics is gaining importance within the field of Molecular Ecology, because of its novel evolutionary implications. Linking population ecology to the variation in epigenetic profiles can help explain the effect of environmental conditions on phenotypic differences among populations. While epigenetic changes have largely been investigated through the examination of DNA methylation under laboratory conditions, there is a limited understanding of the extent of DNA methylation variation in wild populations. Assuming that epigenetic variation is important in nature, the conditions experienced by different conspecific populations should result in levels of DNA methylation that are independent of their genetic differentiation. To test this, we investigated levels of DNA methylation among populations of the sandhopper Talorchestia capensis that show phenotypic (physiological) differences in their response to environmental conditions, at the same time evaluating their genetic relationships. Given the high levels of inter-individual physiological variation observed within populations, we further hypothesised that inter-individual differences in methylation would be high. Levels of genetic and epigenetic variation were assessed within and among populations from five localities using the methylation sensitive amplified polymorphism technique. Population differentiation was higher for epigenetics than genetics, with no clear geographical pattern or any relation to biogeography. Likewise, individuals showed greater variability in their epigenetic than their genetic profiles. Four out of five populations showed significant negative relationships between epigenetic and genetic diversity. These results show uncoupling between epigenetic and genetic variation and suggest that: (1) epigenetics are more responsive to local, site-specific environmental conditions than genetics and (2) individual differences in epigenetic profiles drive phenotypic variation within (and most likely among) natural populations. Within populations, epigenetics could offer a level of phenotypic flexibility beyond genetic constraint that allows rapid responses to variable or unpredictable environments, potentially compensating for low genetic variability.

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References

  • Alvarado S, Fernald RD, Storey KB, Szyf M (2014) The dynamic nature of DNA methylation: a role in response to social and seasonal variation. Integr Comp Biol 54(1):68–76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA + for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth

    Google Scholar 

  • 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 19:1283–1295

    Article  CAS  PubMed  Google Scholar 

  • Azzi A, Dallmann R, Casserly A, Rehrauer H, Patrignani A, Maier B, Kramer A, Brown SA (2014) Circadian behavior is light-reprogrammed by plastic DNA methylation. Nat Neurosci 17:377–382

    Article  CAS  PubMed  Google Scholar 

  • Baldanzi S, McQuaid CD, Cannicci S, Porri F (2013) Environmental domains and range-limiting mechanisms: testing the Abundant Centre Hypothesis using Southern African sandhoppers. PLoS ONE 8(1):e54598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baldanzi S, Weidberg N, Fusi M, Cannicci S, McQuaid CD, Porri F (2015a) Contrasting environments shape thermal physiology across the spatial range of the sandhopper Talorchestia capensis. Oecologia 179:1067–1078

    Article  PubMed  Google Scholar 

  • Baldanzi S, McQuaid CD, Porri F (2015b) Temperature effects on reproductive allocation in the sandhopper Talorchestia capensis. Biol Bull 228:181–191

    Article  PubMed  Google Scholar 

  • Blouin MS, Thuillier V, Cooper B (2010) No evidence for large differences in genomic methylation between wild and hatchery steelhead (Oncorhynchus mykiss). Can J Fish Aquat Sci 67:217–224

    Article  CAS  Google Scholar 

  • Bonin A, Bellemain E, Eidesen PB, Pompanon F, Brochmann C, Taberlet P (2004) How to track and assess genotyping errors in population genetic studies. Mol Ecol 13:3261–3273

    Article  CAS  PubMed  Google Scholar 

  • Bonin A, Ehrich D, Manel S (2007) Statistical analysis of amplified fragment length polymorphism data: a toolbox for molecular ecologists and evolutionists. Mol Ecol 16:3737–3758

    Article  CAS  PubMed  Google Scholar 

  • Bossdorf O, Richards CL, Pigliucci M (2008) Epigenetics for ecologist. Ecol Lett 11:106–115

    PubMed  Google Scholar 

  • Cervera MT, Ruiz-Garcia L, Martinez-Zapater J (2002) Analysis of DNA methylation in Arabidopsis thaliana based on methylation-sensitive AFLP markers. Mol Genet Genomics 268:543–552

    Article  CAS  PubMed  Google Scholar 

  • Dahl E (1946) The Amphipoda of the sound. Part 1. Terrestrial Amphipoda. Acta Univ Lund NF Adv 242:1–53

    Google Scholar 

  • Daxinger L, Whitelaw E (2010) Transgenerational epigenetic inheritance: more questions than answers. Genome Res 20:1623–1628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fulneček J, Kovařik A (2014) How to interpret methylation sensitive amplified polymorphism (MSAP) profiles? BMC Genet 15:2

    Article  PubMed  PubMed Central  Google Scholar 

  • Gavery MR, Roberts SB (2010) DNA methylation patterns provide insight into epigenetic regulation in the Pacific oyster (Crassostrea gigas). BMC Genom 11:483

    Article  Google Scholar 

  • Glastad KM, Hunt BG, Yi SV, Goodisman MAD (2011) DNA methylation in insects: on the brink of the epigenomic era. Insect Mol Biol 20:553–565

    Article  CAS  PubMed  Google Scholar 

  • Glastad KM, Hunt BG, Yi SV, Goodisman MAD (2014) Evolutionary insights into DNA methylation in insects. Curr Opin Insect Sci 1:25–30

    Article  Google Scholar 

  • Griffiths CL, Robinson TB, Lange L, Mead A (2010) Marine biodiversity in South Africa: an evaluation of current states of knowledge. PLoS ONE 5(8):e12008

    Article  PubMed  PubMed Central  Google Scholar 

  • Herrera CM, Bazaga P (2008) Population-genomic approach reveals adaptive floral divergence in discrete populations of a hawk moth pollinated violet. Mol Ecol 17:5378–5390

    Article  CAS  PubMed  Google Scholar 

  • Herrera CM, Bazaga P (2010) Epigenetic differentiation and relationship to adaptive genetic divergence in discrete populations of the violet Viola cazorlensis. New Phytol 187:867–876

    Article  CAS  PubMed  Google Scholar 

  • Herrera CM, Bazaga P (2011) Untangling individual variation in natural populations: ecological, genetic and epigenetic correlates of long-term inequality in herbivory. Mol Ecol 20:1675–1688

    Article  CAS  PubMed  Google Scholar 

  • Herrera CM, Medrano M, Bazaga P (2014) Variation in DNA methylation transmissibility, genetic heterogeneity and fecundity-related traits in natural populations of the perennial herb Helleborus foetidus. Mol Ecol 23:1085–1095

    Article  CAS  PubMed  Google Scholar 

  • Jablonka E, Lamb MJ (1989) The inheritance of acquired epigenetic variations. J Theor Biol 139:69–83

    Article  CAS  PubMed  Google Scholar 

  • Jablonka E, Lamb MJ (1998) Epigenetic inheritance in evolution. J Evol Biol 11:159–183

    Article  Google Scholar 

  • Jablonka E, Lamb MJ (2005) Evolution in four dimensions: genetic, epigenetic, behavioral, and symbolic variation in the history of life. MIT Press, Cambridge

    Google Scholar 

  • Kück P, Greve C, Misof B, Gimnich F (2012) Automated masking of AFLP markers improves reliability of phylogenetic analyses. PLoS ONE 7(11):e49119. doi:10.1371/journal.pone.0049119

    Article  PubMed  PubMed Central  Google Scholar 

  • Liebl AL, Schrey AW, Richards CL, Martin LB (2013) Patterns of DNA methylation throughout a range expansion of an introduced songbird. Integr Comp Biol 53:351–358

    Article  CAS  PubMed  Google Scholar 

  • 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(4):e10326

    Article  PubMed  PubMed Central  Google Scholar 

  • Lu Y, Rong T, Cao M (2008) Analysis of DNA methylation in different maize tissues. J Genet Genomics 35:41–48

    Article  PubMed  Google Scholar 

  • Lyko F, Ramsahoye BH, Jaenisch R (2000) DNA methylation in Drosophila melanogaster. Nature 408:538–540

    Article  CAS  PubMed  Google Scholar 

  • Mandrioli M, Volpi N (2003) The genome of the lepidopteran Mamestra brassicae has a vertebrate-like content of methyl-cytosine. Genetica 119:187–191

    Article  CAS  PubMed  Google Scholar 

  • Massicotte R, Angers B (2012) General-purpose genotype or how epigenetics extend the flexibility of a genotype. Gen Res Int. doi:10.1155/2012/317175

    Google Scholar 

  • Massicotte R, Whitelaw E, Angers B (2011) DNA methylation: a source of random variation in natural populations. Epigenetics 6:421–427

    Article  CAS  PubMed  Google Scholar 

  • Morán P, Pérez-Figueroa A (2011) Methylation changes associated with early maturation stages in the Atlantic salmon. BMC Genet 12:86

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Neill JS, Lee KD, Zhang L, Feeney K, Webster SG, Blades MJ, Kyriacou CP, Hastings MH, Wilcockson DC (2015) Metabolic molecular markers of the tidal clock in the marine crustacean Eurydice pulchra. Curr Biol 25:301–327

    Article  Google Scholar 

  • Pérez-Figueroa A (2013) MSAP: a tool for the statistical analysis of methylation sensitive amplified polymorphism data. Mol Ecol Resources 13:522–527

    Article  Google Scholar 

  • Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev Gen 6:847–859

    Article  CAS  Google Scholar 

  • Reyna-Lopez G, 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 Genet Genomics 253:703–710

    Article  CAS  Google Scholar 

  • Richards EJ (2006) Inherited epigenetic variation—revisiting soft inheritance. Nat Rev Gen 7:395–401

    Article  CAS  Google Scholar 

  • Richards CL, Bossdorf O, Verhoeven KJF (2010) Understanding natural epigenetic variation. New Phytol 187:562–564

    Article  PubMed  Google Scholar 

  • Rivière G (2014) Epigenetic features in the oyster Crassostrea gigas suggestive of functionally relevant promoter DNA methylation in invertebrates. Front Physiol 5:1–7

    Google Scholar 

  • Róis AS, Rodríguez López CM, Cortinhas A, Erben M, Espírito-Santo D, Wilkinson MJ, Caperta AD (2013) Epigenetic rather than genetic factors may explain phenotypic divergence between coastal populations of diploid and tetraploid Limonium spp. (Plumbaginaceae) in Portugal. BMC Plant Biol 13:205

    Article  PubMed  PubMed Central  Google Scholar 

  • Salmon A, Clotault J, Jenczewski E, Chable V, Manzanares-Dauleux MJ (2008) Brassica oleracea displays a high level of DNA methylation polymorphism. Plant Sci 174:61–70

    Article  CAS  Google Scholar 

  • Schrey AW, Coon CAC, Grispo MT, Awad M, Imboma T, McCoy ET, Mushinsky HR, Richards CL, Martin LB et al (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. Article ID 197975

  • Schrey AW, Alvarez M, Foust CM, Kilvitis HJ, Lee JD, Liebl AL, Martin LB, Richards CL, Robertson M (2013) Ecological epigenetics: beyond MS-AFLP. Integr Comp Biol. doi:10.1093/icb/ict012 

    Google Scholar 

  • Schulz B, Eckstein RL, Durka W (2013) Scoring and analysis of methylation-sensitive amplification polymorphisms for epigenetic population studies. Mol Ecol Res 13:642–653

    Article  CAS  Google Scholar 

  • Sun Y, Hou R, Fu X, Sun C, Wang S, Wang C, Li N, Zang L, Bao Z (2014) Genome-wide analysis of DNA methylation in five tissues of zhikong scallop, Chlamys farreri. PLoS ONE 9(1):e86232. doi:10.1371/journal.pone.0086232

    Article  PubMed  PubMed Central  Google Scholar 

  • Teske PR, Zardi GI, McQuaid CD, Nicastro KR (2013) Two sides of the same coin: extinctions and originations across the Atlantic/Indian Ocean boundary as consequences of the same climate oscillation. Front Biogeogr 5:48–59

    Google Scholar 

  • Tricker PJ, Gibbings GJ, Rodiguez-Lopez CM, Hadley P, Wilkinson MJ (2012) Low relative humidity triggers RNA-directed de novo DNA methylation and suppression of genes controlling stomatal development. J Exp Bot. doi:10.1093/jxb/ers076

    PubMed  PubMed Central  Google Scholar 

  • Vogt G, Huber M, Thiemann M, van den Boogaart G, Schmitz OJ, Schubart CD (2008) Production of different phenotypes from the same genotype in the same environment by developmental variation. J Exp Biol 211:510–523

    Article  CAS  PubMed  Google Scholar 

  • Vos P, Hogers R, Bleeker M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wildish DJ (1970) Some factors affecting the distribution of Orchestia Leach in estuaries. J Exp Mar Biol Ecol 5:276–284

    Article  Google Scholar 

  • Wolffe AP, Matzke MA (1999) Epigenetics: regulation through repression. Science 286:481–486

    Article  CAS  PubMed  Google Scholar 

  • Yaish MW, Peng M, Rothstein SJ (2014) Global DNA methylation analysis using methyl-sensitive amplification polymorphism (MSAP). In: Sanchez-Serrano JJ, Salinas J (eds) Arabidopsis protocols, methods in molecular biology, vol 1062. Springer, New York

    Google Scholar 

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Acknowledgements

The authors thank Ms Taryn Bodill from the South African Institute for Aquatic Biodiversity for the analysis of the DNA fragments, and for providing valuable assistance during the laboratory work.

Funding

This paper was written under the framework of the project ‘‘CREC’’ [EU IRSES#247514]. The work is based upon research supported by the National Research Foundation of South Africa (NRF) and the South African Research Chairs Initiative of the Department of Science and Technology.

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Correspondence to Simone Baldanzi.

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Baldanzi, S., Watson, R., McQuaid, C.D. et al. Epigenetic variation among natural populations of the South African sandhopper Talorchestia capensis . Evol Ecol 31, 77–91 (2017). https://doi.org/10.1007/s10682-016-9877-9

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