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Comparative epigenetic and genetic spatial structure in Mediterranean mountain plants: a multispecies study

Heredity volume 132, pages 106–116 (2024)Cite this article

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Abstract

Changes in epigenetic states can allow individuals to cope with environmental changes. If such changes are heritable, this may lead to epigenetic adaptation. Thus, it is likely that in sessile organisms such as plants, part of the spatial epigenetic variation found across individuals will reflect the environmental heterogeneity within populations. The departure of the spatial epigenetic structure from the baseline genetic variation can help in understanding the value of epigenetic regulation in species with different breadth of optimal environmental requirements. Here, we hypothesise that in plants with narrow environmental requirements, epigenetic variability should be less structured in space given the lower variability in suitable environmental conditions. We performed a multispecies study that considered seven pairs of congeneric plant species, each encompassing a narrow endemic with habitat specialisation and a widespread species. In three populations per species we used AFLP and methylation-sensitive AFLP markers to characterise the spatial genetic and epigenetic structures. Narrow endemics showed a significantly lower epigenetic than genetic differentiation between populations. Within populations, epigenetic variation was less spatially structured than genetic variation, mainly in narrow endemics. In these species, structural equation models revealed that such pattern was associated to a lack of correlation between epigenetic and genetic information. Altogether, these results show a greater decoupling of the spatial epigenetic variation from the baseline spatial genetic pattern in endemic species. These findings highlight the value of studying genetic and epigenetic spatial variation to better understand habitat specialisation in plants.

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Fig. 1: Spatial genetic (SGS) and epigenetic (SEGS) structures.
Fig. 2: Geographical location of the studied populations at the Natural Park of Sierras de Cazorla, Segura y Las Villas in south-eastern Peninsula Iberica.
Fig. 3: Genetic and epigenetic structure between populations.
Fig. 4: Spatial distribution of sampled individuals and spatial genetic and epigenetic structure in three of the studied populations.
Fig. 5: Summary of the discrepancy between fine-scale genetic and epigenetic spatial structures found in populations of narrow endemics and widespread species.
Fig. 6: Comparison between groups of species (narrow endemics and widespread species) in the relationship between spatial distance, genetic relatedness and epigenetic similarity.

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Data availability

All data are available in Figshare. https://doi.org/10.6084/m9.figshare.24898461.

References

  • Alonso C, Ramos-Cruz D, Becker C (2019) The role of plant epigenetics in biotic interactions. N Phytol 221(2):731–737

    Article  CAS  Google Scholar 

  • Avramidou EV, Ganopoulos IV, Doulis AG, Tsaftaris AS, Aravanopoulos FA (2015) Beyond population genetics: natural epigenetic variation in wild cherry (Prunus avium). Tree Genet Genomes 11(5):95

    Article  Google Scholar 

  • Balao F, Paun O, Alonso C (2018) Uncovering the contribution of epigenetics to plant phenotypic variation in Mediterranean ecosystems. Plant Biol 20:38–49

    Article  PubMed  Google Scholar 

  • Barrett SCH, Kohn JR (1991) Genetic and evolutionary consequences of small population size. In: Falk DA, Holsinger KE (eds) Genetics and conservation of rare plants. Oxford University Press, Oxford, pp 3–30

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48

    Article  Google Scholar 

  • Blanca G, Cabezudo B, Cueto M, Fernández López C, Morales Torres C (2009) Flora Vascular de Andalucía Oriental, 4 vols. Consejería de Medio Ambiente, Junta de Andalucía, Sevilla

  • Castilla AR, Alonso C, Herrera CM (2012) Genetic structure of the shrub Daphne laureola across the Baetic Ranges, a Mediterranean glacial refugium and biodiversity hotspot. Plant Biol 14:515–524

    Article  CAS  PubMed  Google Scholar 

  • Cavers S, Degen B, Caron H, Lemes MR, Margis R, Salgueiro F et al. (2005) Optimal sampling strategy for estimation of spatial genetic structure in tree populations. Heredity 95:281–289

    Article  CAS  PubMed  Google Scholar 

  • Chybicki IJ, Oleksa A, Burczyk J (2011) Increased inbreeding and strong kinship structure in Taxus baccata estimated from both AFLP and SSR data. Heredity 107:589–600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daco L, Matthies D, Hermant S, Colling G (2022) Genetic diversity and differentiation of populations of Anthyllis vulneraria along elevational and latitudinal gradients. Eco Evol 12:e9167

    Article  Google Scholar 

  • De-Lucas AI, González-Martínez SC, Vendramin GG, Hidalgo E, Heuertz M (2009) Spatial genetic structure in continuous and fragmented populations of Pinus pinaster Aiton. Mol Ecol 18(22):4564–4576

    Article  CAS  PubMed  Google Scholar 

  • Doligez A, Baril C, Joly HI (1998) Fine‐scale spatial genetic structure with nonuniform distribution of individuals. Genetics 148:905–919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dray S, Dufour A (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Soft 22:1–20

    Article  Google Scholar 

  • Dubin MJ, Zhang P, Meng D, Remigereau M-S, Osborne EJ, Casale FP et al. (2015) DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation. ELife 4:e05255

    Article  PubMed  PubMed Central  Google Scholar 

  • Eckstein RL, O’Neill RA, Danihelka J, Otte A, Köhler W (2006) Genetic structure among and within peripheral and central populations of three endangered floodplain violets. Mol Ecol 15:2367–2379

    Article  CAS  PubMed  Google Scholar 

  • Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242

    Article  Google Scholar 

  • Ennos R (2001) Inferences about spatial processes in plant populations from the analysis of molecular markers. In: Silvertown J, Antonovics J (eds) Integrating ecology and evolution in a spatial context. Blackwell Science, London, pp 45–72

  • Epperson BK (2005) Estimating dispersal from short distance spatial autocorrelation. Heredity 95:7–15

    Article  CAS  PubMed  Google Scholar 

  • Feng S, Jacobsen SE, Reik W (2010) Epigenetic reprogramming in plant and animal development. Science 330:622–627

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Fernández-Mazuecos M, Jiménez-Mejías P, Rotllan-Puig X, Vargas P (2014) Narrow endemics to Mediterranean islands: moderate genetic diversity but narrow climatic niche of the ancient, critically endangered Naufraga (Apiaceae). Perspect Plant Ecol Evol Syst 16(4):190–202

    Article  Google Scholar 

  • Forrest A, Escudero M, Heuertz M, Wilson Y, Cano E, Vargas P (2017) Testing the hypothesis of low genetic diversity and population structure in narrow endemic species: the endangered Antirrhinum charidemi (Plantaginaceae). Bot J Linn Soc 183:260–270

    Article  Google Scholar 

  • Foust CM, Preite V, Schrey AW, Alvarez M, Robertson MH, Verhoeven KJF et al. (2016) Genetic and epigenetic differences associated with environmental gradients in replicate populations of two salt marsh perennials. Mol Ecol 25(8):1639–1652

    Article  CAS  PubMed  Google Scholar 

  • Fulneček J, Kovařík A (2014) How to interpret methylation sensitive amplified polymorphism (MSAP) profiles? BMC Genet 15:2–9

    Article  PubMed  PubMed Central  Google Scholar 

  • Gamba D, Muchhala N (2020) Global patterns of population genetic differentiation in seed plants. Mol Ecol 29:3413–3428

    Article  CAS  PubMed  Google Scholar 

  • Gamba D, Muchhala N (2022) Pollinator type strongly impacts gene flow within and among plant populations for six Neotropical species. Ecology 104(1):e3845

    Article  PubMed  Google Scholar 

  • Gao L, Geng Y, Li B, Chen J, Yang J (2010) Genome-wide DNA methylation alterations of Alternanthera philoxeroides in natural and manipulated habitats: Implications for epigenetic regulation of rapid responses to environmental fluctuation and phenotypic variation. Plant Cell Environ 33:1820–1827

    Article  CAS  PubMed  Google Scholar 

  • Gapare WJ, Aitken SN (2005) Strong spatial genetic structure in peripheral but not core populations of Sitka spruce [Picea sitchensis (Bong.) Carr.]. Mol Ecol 14:2659–2667

    Article  CAS  PubMed  Google Scholar 

  • García-Castaño JL, Balao F, Lorenzo MT, Vela E, Hadjadj-Aoul S, Mifsud S et al. (2021) A complex genetic structure of Tetraclinis articulata (Cupressaceae) in the western Mediterranean. Bot J Linn Soc 197(3):420–438

    Article  Google Scholar 

  • Gáspár B, Bossdorf O, Durka W (2018) Structure, stability and ecological significance of natural epigenetic variation: a large-scale survey in Plantago lanceolata. N. Phytol 221:1585–1596

    Article  Google Scholar 

  • Gitzendanner MA, Soltis PS (2000) Patterns of genetic variation in rare and widespread plant congeners. Am J Bot 87(6):783–792

    Article  CAS  PubMed  Google Scholar 

  • Guan Y, Qu P, Lu S, Crabbe M, Zhang T, Geng Y (2020) Spatial genetic and epigenetic structure of Thlaspi arvense (field pennycress) in China. Genes Genet Syst 95(5):225–234

    Article  CAS  PubMed  Google Scholar 

  • Hamrick JL, Trapnell DW (2011) Using population genetic analyses to understand seed dispersal patterns. Acta Oecol 37:641–649

    Article  ADS  Google Scholar 

  • Hardy OJ (2003) Estimation of pairwise relatedness between individuals and characterisation of isolation by distance processes using dominant genetic markers. Mol Ecol 12:1577–1588

    Article  PubMed  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Hardy OJ, Maggia L, Bandou E, Breyne P, Caron H, Chevallier MH et al. (2006) Fine-scale genetic structure and gene dispersal inferences in 10 Neotropical tree species. Mol Ecol 15:559–571

    Article  CAS  PubMed  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(24):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. N. Phytol 187(3):867–876

    Article  CAS  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, Bazaga P (2016) Genetic and epigenetic divergence between disturbed and undisturbed subpopulations of a Mediterranean shrub: a 20-year field experiment. Ecol Evol 6(11):3832–3847

    Article  PubMed  PubMed Central  Google Scholar 

  • Herrera CM, Medrano M, Bazaga P (2016) Comparative spatial genetics and epigenetics of plant populations: Heuristic value and a proof of concept. Mol Ecol 25:1653–1664

    Article  CAS  PubMed  Google Scholar 

  • Herrera CM, Medrano M, Bazaga P (2017) Comparative epigenetic and genetic spatial structure of the perennial herb Helleborus foetidus: Isolation by environment, isolation by distance, and functional trait divergence. Am J Bot 104(8):1195–1204

    Article  PubMed  Google Scholar 

  • Ibañez VN, Masuelli RW, Marfil CF (2021) Environmentally induced phenotypic plasticity and DNA methylation changes in a wild potato growing in two contrasting Andean experimental gardens. Heredity 126:50–62

    Article  PubMed  Google Scholar 

  • Jablonka E, Raz G (2009) Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q Rev Biol 84(2):131–177

    Article  PubMed  Google Scholar 

  • Jiménez‐Mejías P, Fernández‐Mazuecos M, Amat ME, Vargas P (2015) Narrow endemics in European mountains: high genetic diversity within the monospecific genus Pseudomisopates (Plantaginaceae) despite isolation since the late Pleistocene. J Biogeogr 42(8):1455–1468

    Article  Google Scholar 

  • Johannes F, Schmitz RJ (2019) Spontaneous epimutations in plants. N. Phytol 221:1253–1259

    Article  Google Scholar 

  • Jump AS, Penuelas J (2007) Extensive spatial genetic structure revealed by AFLP but not SSR molecular markers in the wind‐pollinated tree, Fagus sylvatica. Mol Ecol 16(5):925–936

    Article  CAS  PubMed  Google Scholar 

  • Kawakatsu T, Huang S-SC, Jupe F, Sasaki E, Schmitz RJ, Urich MA et al. (2016) Epigenomic diversity in a global collection of Arabidopsis thaliana accessions. Cell 166:492–505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim NS, Im MJ, Nkongolo K (2016) Determination of DNA methylation associated with Acer rubrum (red maple) adaptation to metals: Analysis of global DNA modifications and methylation‐sensitive amplified polymorphism. Ecol Evol 6(16):5749–5760

    Article  PubMed  PubMed Central  Google Scholar 

  • Lara-Romero, García-Fernandez C, Robledo-Arnuncio A, Roumet JJ, Morente-Lopez M, Lopez-Gil A et al. (2016) Individual spatial aggregation correlates with between-population variation in fine-scale genetic structure of Silene ciliata (Caryophyllaceae). Heredity 116:417–423

    Article  CAS  PubMed  Google Scholar 

  • Lavergne S, Thompson JD, Garnier E, Debussche M (2004) The biology and ecology of narrow endemic and widespread plants: a comparative study of trait variation in 20 congeneric pairs. Oikos 107(3):505–518

    Article  ADS  Google Scholar 

  • Lefcheck JS (2016) piecewiseSEM: Piecewise structural equation modeling in R for ecology, evolution, and systematics. Methods Ecol Evol 7(5):573–579

    Article  Google Scholar 

  • Legendre P (1993) Spatial autocorrelation: trouble or new paradigm? Ecology 74:1659–1673

    Article  Google Scholar 

  • Lehmair TA, Poschlod P, Reisch C (2022) The impact of environment on genetic and epigenetic variation in Trifolium pratensepopulations from two contrasting semi-naturalgrasslands. R Soc Open Sci 9:211406

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Lele L, Ning D, Cuiping P, Xiao G, Weihua G (2018) Genetic and epigenetic variations associated with adaptation to heterogeneous habitat conditions in a deciduous shrub. Ecol Evol 8(5):2594–2606

    Article  PubMed  PubMed Central  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 5:1–8

  • Luzuriaga AL, González JM, Escudero A (2015) Annual plant community assembly in edaphically heterogeneous environments. J Veg Sci 26(5):866–875

    Article  Google Scholar 

  • Medrano M, Herrera CM, Bazaga P (2014) Epigenetic variation predicts regional and local intraspecific functional diversity in a perennial herb. Mol Ecol 23:4926–4938

    Article  CAS  PubMed  Google Scholar 

  • Medrano M, Alonso C, Bazaga P, López E, Herrera CM (2020) Comparative genetic and epigenetic diversity in pairs of sympatric, closely related plants with contrasting distribution ranges in south-eastern iberian mountains. AoB Plants 12(3):plaa013

    Article  PubMed  PubMed Central  Google Scholar 

  • Murphy MV (2022) semEff: automatic calculation of effects for Piecewise Structural Equation Models. R package version 0.6.1. https://CRAN.R-project.org/package=semEff

  • Nagamitsu T, Shuri K, Kikuchi S, Koike S, Naoe S, Masaki T (2019) Multiscale spatial genetic structure within and between populations of wild cherry trees in nuclear genotypes and chloroplast haplotypes. Ecol Evol 9(19):11266–11276

    Article  PubMed  PubMed Central  Google Scholar 

  • Nicotra AB, Segal DL, Hoyle GL, Schrey AW, Verhoeven KJF, Richards CL (2015) Adaptive plasticity and epigenetic variation in response to warming in an Alpine plant. Ecol Evol 5:634–647

    Article  PubMed  PubMed Central  Google Scholar 

  • Noshay JM, Springer NM (2021) Stories that can’t be told by SNPs; DNA methylation variation in plant populations. Curr Opin Plant Biol 61:101989

    Article  CAS  PubMed  Google Scholar 

  • Osuna‐Mascaró C, Agneray AC, Galland LM, Leger EA, Parchman TL (2023) Fine‐scale spatial genetic structure in a locally abundant native bunchgrass (Achnatherum thurberianum) including distinct lineages revealed within seed transfer zones. Evol Appl 16(5):979–996

    Article  Google Scholar 

  • Pandey M, Rajora OP (2012) Higher fine-scale genetic structure in peripheral than in core populations of a long-lived and mixed-mating conifer - eastern white cedar (Thuja occidentalis L.). BMC Evol Biol 12:1–14

    Article  Google Scholar 

  • Paun O, Bateman RM, Fay MF, Hedren M, Civeyrel L, Chase MW (2010) Stable epigenetic effects impact adaptation in allopolyploid orchids (Dactylorhiza: Orchidaceae). Mol Biol Evol 27(11):2465–2473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paun O, Schönswetter P (2012) Amplified fragment length polymorphism: an invaluable fingerprinting technique for genomic, transcriptomic, and epigenetic studies. Methods Mol Biol 862:75–87

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pescador DS, Cruz M, Chacón‐Labella J, Pavón‐García J, Escudero A (2020) Tales from the underground: soil heterogeneity and not only above‐ground plant interactions explain fine‐scale species patterns in a Mediterranean dwarf‐shrubland. J Veg Sci 31(3):497–508

    Article  Google Scholar 

  • Rabinowitz D (1981) Seven forms of rarity. In: Synge H (ed) Biological aspects of rare plant conservation. John Wiley and Sons, New York, pp 205–217

  • Rendina González AP, Preite V, Verhoeven KJ, Latzel V (2018) Transgenerational effects and epigenetic memory in the clonal plant Trifolium repens. Front Plant Sci 9:1677

    Article  PubMed  PubMed Central  Google Scholar 

  • Reyna-López 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(6):703–710

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Richards CL, Schrey AW, Pigliucci M (2012) Invasion of diverse habitats by few Japanese knotweed genotypes is correlated with epigenetic differentiation. Ecol Lett 15(9):1016–1025

    Article  PubMed  Google Scholar 

  • Rousset F (2000) Genetic differentiation between individuals. J Evol Biol 13:58–62

    Article  Google Scholar 

  • Schouten OS, Houseman GR (2019) Effect of soil heterogeneity and endogenous processes on plant spatial structure. Ecology 100:e02837

    Article  PubMed  Google Scholar 

  • Schrey AW, Alvarez M, Foust CM, Kilvitis HJ, Lee JD, Liebl AL et al. (2013) Ecological epigenetics: beyond MS-AFLP. Integr Comp Biol 53:340–350

    Article  PubMed  Google Scholar 

  • Schulz B, Eckstein RL, Durka W (2014) Epigenetic variation reflects dynamic habitat conditions in a rare floodplain herb. Mol Ecol 23:3523–3537

    Article  PubMed  Google Scholar 

  • Shen J, Wang Z, Su Y, Wang T (2021) Associations between population epigenetic differentiation and environmental factors in the exotic weed mile-a-minute (Mikania micrantha). Weed Sci 69(3):307–332

    Article  Google Scholar 

  • Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47:264–279

    Article  PubMed  Google Scholar 

  • Slatyer RA, Hirst M, Sexton JP (2013) Niche breadth predicts geographical range size: a general ecological pattern. Ecol Lett 16:1104–1114

    Article  PubMed  Google Scholar 

  • Stone BW, Ward A, Farenwald M, Lutz AW, Wolfe AD (2019) Genetic diversity and population structure in Cary’s Beardtongue Penstemon caryi (Plantaginaceae), a rare plant endemic to the eastern Rocky Mountains of Wyoming and Montana. Conserv Genet 20:1149–1161

    Article  CAS  Google Scholar 

  • Thiebaut F, Hemerly AS, Ferreira PCG (2019) A role for epigenetic regulation in the adaptation and stress responses of non-model plants. Front Plant Sci 10:246

    Article  PubMed  PubMed Central  Google Scholar 

  • Thompson JD, Lavergne S, Affre L, Gaudeul M, Debussche M (2005) Ecological differentiation of Mediterranean endemic plants. Taxon 54(4):967–976

    Article  Google Scholar 

  • Turner BM (2009) Epigenetic responses to environmental change and their evolutionary implications. Philos Trans R Soc Lond B Biol Sci 364:3403–3418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valverde J, Gómez JM, García C, Sharbel TF, Jiménez MN, Perfectti F (2016) Inter-annual maintenance of the fine-scale genetic structure in a biennial plant. Sci Rep. 24(6):37712

    Article  ADS  Google Scholar 

  • Van Antro M, Prelovsek S, Ivanovic S, Gawehns F, Wagemaker NC, Mysara M et al. (2023) DNA methylation in clonal duckweed (Lemna minor L.) lineages reflects current and historical environmental exposures. Mol Ecol 32(2):428–443

    Article  PubMed  Google Scholar 

  • Vekemans X, Beauwens T, Lemaire M, Roldan-Ruiz I (2002) Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Mol Ecol 11:139–151

    Article  CAS  PubMed  Google Scholar 

  • Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935

    Article  CAS  PubMed  Google Scholar 

  • Verhoeven KJF, Jansen JJ, van Dijk PJ, Biere A (2010) Stress-induced DNA methylation changes and their heritability in asexual dandelions. N. Phytol 185:1108–1118

    Article  CAS  Google Scholar 

  • Verhoeven KJF, Von Holdt BM, Sork VL (2016) Epigenetics in ecology and evolution: what we know and what we need to know. Mol Ecol 25:1631–1638

    Article  PubMed  Google Scholar 

  • Volis S, Ormanbekova D, Shulgina I (2016) Fine-scale spatial genetic structure in predominantly selfing plants with limited seed dispersal: a rule or exception? Plant Divers 38(2):59–64

    Article  PubMed  PubMed Central  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M et al. (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23(21):4407–4414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilschut RA, Oplaat C, Snoek LB, Kirschner J, Verhoeven KJF (2016) Natural epigenetic variation contributes to heritable flowering divergence in a widespread asexual dandelion lineage. Mol Ecol 25(8):1759–1768

    Article  CAS  PubMed  Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28(2):114–138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354

    Article  MathSciNet  CAS  PubMed  Google Scholar 

  • Wu WQ, Yi MR, Wang XF, Ma L, Jiang L, Li XW et al. (2013) Genetic and epigenetic differentiation between natural Betula ermanii (Betulaceae) populations inhabiting contrasting habitats. Tree Genet Genomes 9:1321–1328

    Article  Google Scholar 

  • Xue W, Huang L, Yu FH, Bezemer TM (2022) Light condition experienced by parent plants influences the response of offspring to light via both parental effects and soil legacy effects. Funct Ecol 36(10):2434–2444

    Article  CAS  Google Scholar 

  • Yao N, Zhang Z, Yu L, Hazarika R, Yu C, Jang H et al. (2023) An evolutionary epigenetic clock in plants. Science 381(6665):1440–1445

  • Zhang Y-Y, Fischer M, Colot V, Bossdorf O (2012) Epigenetic variation creates potential for evolution of plant phenotypic plasticity. N. Phytol 197(1):314–322

    Article  CAS  Google Scholar 

  • Zilberman D, Gehring M, Tran R, Ballinger T, Henikoff S (2007) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39:61–69

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We are very grateful to Pilar Bazaga and Esmeralda López-Perea for laboratory assistance. Noelia Zara for her help in sampling Erodium individuals. We thank the Consejería de Medio Ambiente, Junta de Andalucía, for authorising this research. This work was supported by the Consejería de Innovación Ciencia y Empresa, Junta de Andalucía [P18-FR-4413] and the Ministerio de Ciencia e Innovación, Spanish Government [PID2019-104365GB-I00/AEI/10.13039/501100011033 and SUMHAL-LIFEWATCH-2019-09-CSIC-4, through European Regional Development Funds POPE 2014-2020].

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  1. Estación Biológica de Doñana, Consejo Superior de Investigaciones Científicas (CSIC), Sevilla, Spain

    Javier Valverde, Mónica Medrano, Carlos M. Herrera & Conchita Alonso

  2. Departamento de Biología Vegetal y Ecología, Universidad de Sevilla, Sevilla, Spain

    Javier Valverde

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CA, CMH and MM designed the methodology and collected the data; CA, CMH, MM and JV elaborated the hypotheses; JV analysed the data and led the writing of the manuscript. All authors contributed to the revision of the manuscript and gave their final approval for publication.

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Correspondence to Javier Valverde or Conchita Alonso.

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Valverde, J., Medrano, M., Herrera, C.M. et al. Comparative epigenetic and genetic spatial structure in Mediterranean mountain plants: a multispecies study. Heredity 132, 106–116 (2024). https://doi.org/10.1038/s41437-024-00668-3

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