Marine Biology

, 165:50 | Cite as

Morphological and epigenetic variation in mussels from contrasting environments

  • R. G. A. Watson
  • Simone Baldanzi
  • A. Pérez-Figueroa
  • G. Gouws
  • F. Porri
Original paper


The impact of contrasting environments on organisms can result in the establishment of distinct phenotypic traits. Environmentally induced epigenetic mechanisms directly regulate gene expression and potentially lead to long-lasting effects. How phenotypic, epigenetic, and genetic components of wild populations relate to each other is, however, still largely debated. We examined the effect of broad coastline topography (as bay versus open coast) on the morphological, genetic, and epigenetic (i.e., DNA methylation) traits of the brown mussel Perna perna from four natural populations along the south coast of South Africa (between 33.9 S, 25.7 E and 34.2 S, 22.1 E) collected in April 2014. Several morphometric measurements were taken on the mussel body and byssal thread. The epigenetic and genetic structure of P. perna was assessed using the methylation sensitive analysis of polymorphisms technique. Morphological traits differed among populations, but no clear effect of topography on both morphology and genetics was found. Bay and Open Coast sites differed in the patterns of DNA methylation of selected loci, suggesting that topography shaped the epigenetic profile of populations of P. perna. The environmentally induced changes in the DNA methylation of selected loci were neither correlated with the morphological traits analysed, nor explained by the underlying genetic variance among populations. The relationship amongst epigenetics, morphology, and genetics of P. perna populations was shown to be complex and dynamic. Although inconsistent, the topographically linked variability in epigenetic and the phenotypic differences in genetically close populations of mussels highlights the potential role of the local environment in driving mesoscale differences among populations.



We thank N. Weidberg, D. Sousoni, and J. Bueno for assistance during the field collection and T. Bodill for assistance in the molecular laboratory. FP wishes to thank Dr Dittmar Eichoff for early discussions on epigenetics and sharing ideas and applications on orthodontics and marine ecology. We finally thank two anonymous reviewers for their valuable contribution on the revision of this paper.


This contribution is based upon research supported by funds provided by the South African Institute for Aquatic Biodiversity.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest

Ethical approval

All applicable international, national, and institutional guidelines for the care and use of animals were followed.

Supplementary material

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Supplementary material 1 (PDF 247 kb)
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Supplementary material 2 (HTML 1056 kb)


  1. Akester RJ, Martel AL (2000) Shell shape, dysodont tooth morphology, and hinge-ligament thickness in the bay mussel Mytilus trossulus correlate with wave exposure. Can J Zool 78(2):240–253. CrossRefGoogle Scholar
  2. Anastasiadi D, Diaz N, Piferrer F (2017) Small ocean temperature increases elicit stage-dependent changes in DNA methylation and gene expression in a fish, the European sea bass. Sci Reports 7:12401. CrossRefGoogle Scholar
  3. 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 9:1283–1295. CrossRefGoogle Scholar
  4. Ardura A, Zaiko A, Morán P, Planes S, Garcia-Vazquez E (2017) Epigenetic signatures of invasive status in populations of marine invertebrates. Sci Reports 7:42193. CrossRefGoogle Scholar
  5. Arribas LP, Donnarumma L, Palomo MG, Scrosati RA (2014) Intertidal mussels as ecosystem engineers: their associated invertebrate biodiversity under contrasting wave exposures. Mar Biodivers 44:203–211. CrossRefGoogle Scholar
  6. Baldanzi S, Watson RGA, McQuaid C, Gouws G, Porri F (2017) Epigenetic variation among natural populations of the South African sandhopper Talorchestia capensis. Evol Ecol 31:77–91CrossRefGoogle Scholar
  7. Balla SA, Walker KF (1991) Shape variation in the Australian freshwater mussel Alathyria jacksoni Iredale (Bivalvia, Hyriidae). Hydrobiol 220:89. CrossRefGoogle Scholar
  8. Baurens F-C, Causse S, Legavre T (2008) Methylation-sensitive amplification polymorphism (MSAP) protocol to assess CpG and CpNpG methylation in the banana genome. Fruits 63:117–123. CrossRefGoogle Scholar
  9. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Methodol 57(1):289–300Google Scholar
  10. Bossdorf O, Richards CL, Pigliucci M (2008) Epigenetics for ecologists. Ecol Let 11:106–115. Google Scholar
  11. Branch GM, Griffiths CL, Branch M, Beckley L (2010) Two Oceans: a guide to the marine life of southern Africa. Struik Nature, GardensGoogle Scholar
  12. Briones C, Rivadeneira MM, Fernandez M, Guiñez R (2014) Geographical variation of shell thickness in the mussel Perumytilus purpuratus along the southeast pacific coast. Biol Bull 227:221–231CrossRefPubMedGoogle Scholar
  13. Brown KM, Quinn JF (1988) The effect of wave action on growth in three species of intertidal gastropods. Oecologia 75:420–425. CrossRefPubMedGoogle Scholar
  14. Bryson ES, Trussell GC, Ewanchuk PJ (2014) Broad-scale geographic variation in the organization of rocky intertidal communities in the Gulf of Maine-. Ecol Monogr 84:579–597CrossRefGoogle Scholar
  15. Caro AU, Escobar J, Bozinovic F, Navarrete SA, Castilla JC (2008) Phenotypic variability in byssus thread production of intertidal mussels induced by predators with different feeding strategies. Mar Ecol Prog Ser 372:127–134. CrossRefGoogle Scholar
  16. Carrington E, Moeser GM, Dimond J, Mello JJ, Boller ML (2009) Seasonal disturbance to mussel beds: field test of a mechanistic model predicting wave dislodgment. Limnol Oceanogr 54:978–986. CrossRefGoogle Scholar
  17. Cole VJ (2010) Alteration of the configuration of bioengineers affects associated taxa. Mar Ecol Prog Ser 416:127–136. CrossRefGoogle Scholar
  18. Cole VJ, McQuaid CD (2010) Bioengineers and their associated fauna respond differently to the effects of biogeography and upwelling. Ecology 91(12):3549–3562. CrossRefPubMedGoogle Scholar
  19. Daxinger L, Whitelaw E (2010) Transgenerational epigenetic inheritance: more questions than answers. Genome Res 20:1623–1628. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620CrossRefPubMedGoogle Scholar
  21. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
  22. Fitzgerald TL, Shapter FM, McDonald S, Waters DLE, Chivers IH, Drenth A, Nevo E, Henry RJ (2011) Genome diversity in wild grasses under environmental stress. Proc Natl Acad Sci 108(52):21140–21145. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Gan J, Allen JS (2002) A modeling study of shelf circulation off northern California in the region of the Coastal Ocean Dynamics Experiment: response to relaxation of upwelling winds. J Geophys Res 107(C9):3123. CrossRefGoogle Scholar
  24. García LV (2004) Escaping the Bonferroni iron claw in ecological studies. Oikos 105(3):657–663. CrossRefGoogle Scholar
  25. Garner YL, Litvaitis MK (2013) Effects of wave exposure, temperature and epibiont fouling on byssal thread production and growth in the blue mussel, Mytilus edulis, in the Gulf of Maine. J Exp Mar Biol Ecol 446:52–56. CrossRefGoogle Scholar
  26. Gavery MR, Roberts SB (2013) Predominant intragenic methylation is associated with gene expression characteristics in a bivalve mollusc. Peer J 1:e215. CrossRefPubMedPubMedCentralGoogle Scholar
  27. Geyer WR, Signell RP (1992) A reassessment of the role of tidal dispersion in estuaries and bays. Estuaries 15:97–108. CrossRefGoogle Scholar
  28. Goschen WS, Schumann EH (1990) Agulhas current variability and inshore structures off the Cape Province, South Africa. J Geophys Res 95:667–678. CrossRefGoogle Scholar
  29. Gracey AY, Chaney ML, Boomhower JP, Tyburczy WR, Connor K, Somero GN (2008) Rhythms of gene expression in a fluctuating intertidal environment. Curr Biol 18:1501–1507. CrossRefPubMedGoogle Scholar
  30. Grant WS, Schneider AC, Leslie RW, Cherry MI (1992) Population genetics of the brown mussel Perna perna in southern Africa. J Exp Mar Biol Ecol 165:45–58. CrossRefGoogle Scholar
  31. Gu Z, Eils R, Schlesner M (2016) Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 32:2847–2849. CrossRefPubMedGoogle Scholar
  32. Hammond W, Griffiths CL (2004) Influence of wave exposure on South African mussel beds and their associated infaunal communities. Mar Biol 144:547–552. CrossRefGoogle Scholar
  33. Hoffmann AA, Willi Y (2008) Detecting genetic responses to environmental change. Nature 9:421–432Google Scholar
  34. Hofmann GE (2017) Ecological epigenetics in Marine Metazoans. Front Mar Sci 4:4. CrossRefGoogle Scholar
  35. Jablonka E, Lamb MJ (1998) Epigenetic inheritance in evolution. J Evolution Biol 11(2):159–183CrossRefGoogle Scholar
  36. Jablonka E, Lamb MJ (2005) Evolution in four dimensions: genetic, epigenetic, behavioral, and symbolic variation in the history of life. MIT Press, CambridgeGoogle Scholar
  37. Kageyama S, Shinmura K, Yamamoto H, Goto M, Suzuki K, Tanioka F, Tsuneyoshi T, Sugimura H (2008) Fluorescence-labeled methylation-sensitive amplified fragment length polymorphism (FL-MS-AFLP) analysis for quantitative determination of DNA methylation and demethylation status. Jpn J Clin Oncol 38(4):317–322. CrossRefPubMedGoogle Scholar
  38. Katolikova M, Khaitov V, Väinölä R, Gantsevich M, Strelkov P (2016) Genetic, ecological and morphological distinctness of the blue mussels Mytilus trossulus Gould and M. edulis L. in the white sea. PLoS One 11(4):e0152963. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Kingsbury JM (1962) The effect of waves on the composition of a population of attached marine algae. Bull Torrey Bot Club 89:143–160. CrossRefGoogle Scholar
  40. Kroeker KJ, Sanford E, Rose JM, Blanchette CA, Chan F, Chavez FP, Gaylord B, Helmuth B, Hill TM, Hofmann GE, McManus MA, Menge BA, Nielsen KJ, Raimondi PT, Russell AD, Washburn L (2016) Interacting environmental mosaics drive geographic variation in mussel performance and predation vulnerability. Ecol Lett 19:771–779CrossRefPubMedGoogle Scholar
  41. 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. CrossRefPubMedGoogle Scholar
  42. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  43. Liu S, Sun K, Jiang T, Ho JP, Liu B, Feng J (2012) Natural epigenetic variation in the female great roundleaf bat (Hipposideros armiger) populations. Mol Genet Genom 287:643–650. CrossRefGoogle Scholar
  44. López MS, Coutinho R, Ferreira CEL, Rilov G (2010) Predator–prey interactions in a bioinvasion scenario: differential predation by native predators on two exotic rocky intertidal bivalves. Mar Ecol Prog Ser 403:101–112. CrossRefGoogle Scholar
  45. Marsh AG, Pasqualone AA (2014) DNA methylation and temperature stress in an Antartic polychete, Spiophanes tcherniai. Front Physiol 5:173. CrossRefPubMedPubMedCentralGoogle Scholar
  46. Massicotte R, Whitelaw E, Angers B (2011) DNA methylation: a source of random variation in natural populations. Epigenetics 6:421–427. CrossRefPubMedGoogle Scholar
  47. McQuaid CD, Phillips TE (2000) Limited wind-driven dispersal of intertidal mussel larvae: in situ evidence from the plankton and the spread of the invasive species Mytilus galloprovincialis in South Africa. Mar Ecol Prog Ser 201:211–220. CrossRefGoogle Scholar
  48. Metzger DCH, Schulte PM (2017) Persistent and plastic effects of temperature on DNA methylation across the genome of threespine stickleback (Gasterosteus aculeatus). Proc R Soc Lond B. Google Scholar
  49. Navarrete SA, Wieters EA, Broitman BR, Castilla JC (2005) Scales of bentho-pelagic coupling and the intensity of species interactions: from recruitment limitation to top-down control. PNAS 102:18046–18051. CrossRefPubMedPubMedCentralGoogle Scholar
  50. Nicastro KR, Zardi GI, McQuaid CD, Teske PR, Barker NP (2008) Coastal topography drives genetic structure in marine mussels. Mar Ecol Prog Ser 368:189–195CrossRefGoogle Scholar
  51. Nicastro KR, Zardi GI, McQuaid CD (2010) Differential reproductive investment, attachment strength and mortality of invasive and indigenous mussels across heterogeneous environments. Biol Inv 12:2165–2177CrossRefGoogle Scholar
  52. Pérez-Figueroa A (2013) msap: a tool for the statistical analysis of methylation-sensitive amplified polymorphism data. Mol Ecol 13:522–527. CrossRefGoogle Scholar
  53. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  54. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  55. Reimer O, Tedengren M (1996) Phenotypical improvement of morphological defences in the mussel Mytilus edulis induced by exposure to the predator Asterias rubens. Oikos. Google Scholar
  56. Richards EJ (2006) Inherited epigenetic variation—revisiting soft inheritance. Nature Rev Genetics 7:395–401. CrossRefGoogle Scholar
  57. Richards CL, Bossdorf O, Verhoeven KJ (2010) Understanding natural epigenetic variation. New Phytol 187:562–564. CrossRefPubMedGoogle Scholar
  58. Schaeffer-Novelli Y, Cintrón-Molero G, Adaime R, Camargo T (1990) Variability of mangrove ecosystems along the Brazilian coast. Estuaries 13:204–218. CrossRefGoogle Scholar
  59. Siegfried WR, Hockey PAR, Crowe AA (1985) Exploitation and conservation of brown mussel stocks by coastal people of Transkei. Environ Conserv 12:303–307. CrossRefGoogle Scholar
  60. Skinner MK, Manikkam M, Guerrero-Bosagna C (2010) Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol Metab 21(4):214–222. CrossRefPubMedPubMedCentralGoogle Scholar
  61. Sorte CJB, Jones SJ, Miller LP (2011) Geographic variation in temperature tolerance as an indicator of potential population responses to climate change. J Exp Mar Biol Ecol 400:209–217CrossRefGoogle Scholar
  62. StatSoft Inc (2012) STATISTICA (data analysis software system), version 12.0.
  63. Steffani CN, Branch GM (2003) Growth rate, condition, and shell shape of Mytilus galloprovincialis: responses to wave exposure. Mar Ecol Prog Ser 246:197–209. CrossRefGoogle Scholar
  64. Su Z, Han L, Zhao Z (2011) Conservation and divergence of DNA methylation in eukaryotes: new insights from single base-resolution DNA methylomes. Epigenetics 6:134–140. CrossRefPubMedPubMedCentralGoogle Scholar
  65. Suchanek TH (1985) Mussels and their role in structuring rocky shore communities. In: Moore PG, Seed R (eds) The ecology of rocky coasts. Hodder and Stoughton Press, London, pp 70–96Google Scholar
  66. Tagliarolo M, McQuaid CD (2016) Field measurements indicate unexpected, serious underestimation of mussel heart rates and thermal tolerance by laboratory studies. PLoS One 11(2):e0146341. CrossRefPubMedPubMedCentralGoogle Scholar
  67. Trucchi E, Mazzarella AB, Gilfillan GD, Lorenzo MT, Schönswetter P, Paun O (2016) BsRADseq: screening DNA methylation in natural populations of non-model species. Molec Ecol 25:1697–1713CrossRefGoogle Scholar
  68. Tunley K (2009) State of management of South Africa’s Marine protected areas. WWF South Africa report series—2009/Marine/001, pp 1–209Google Scholar
  69. Underwood AJ (1997) Experiments in ecology. Their logical design and interpretation using analysis of variance. Cambridge University Press, CambridgeGoogle Scholar
  70. Underwood AJ, Chapman MG (1998) Variation in algal assemblages on wave-exposed rocky shores in New South Wales. Mar Fresh Res 49:241–254CrossRefGoogle Scholar
  71. Underwood AJ, Keough MJ (2001) Supply-side ecology: the nature and consequences of variations in recruitment of intertidal organisms. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer Associates, Sunderland, pp 183–200Google Scholar
  72. Unternaehrer E, Luers P, Mill J, Dempster E, Meyer A, Staehli S, Lieb R, Hellhammer DH, Meinlschmidt G (2012) Dynamic changes in DNA methylation of stress-associated genes (OXTR, BDNF) after acute psychosocial stress. Transl Psychiat 2:e150. CrossRefGoogle Scholar
  73. Valdovinos C, Pedrero P (2007) Geographic variations in shell growth rates of the mussel Diplodon chilensis from temperate lakes of Chile: implications for biodiversity conservation. Limnologica 37:63–75CrossRefGoogle Scholar
  74. von der Meden CEO, Porri F, Erlandsson J, McQuaid CD (2008) Coastline topography affects the distribution of indigenous and invasive mussels. Mar Ecol Prog Ser 372:135–145CrossRefGoogle Scholar
  75. Winer BJ (1971) Statistical principles in experimental designs, 2nd edn. McGraw-Hill–Kogakusha, TokyoGoogle Scholar
  76. Zardi GI, Nicastro KR, McQuaid CD, Rius M, Porri F (2006) Hydrodynamic stress and habitat partitioning between indigenous (Perna perna) and invasive (Mytilus galloprovincialis) mussels: constraints of an evolutionary strategy. Mar Biol 150:79–88. CrossRefGoogle Scholar
  77. Zardi GI, Nicastro KR, McQuaid CD, Gektidis M (2009) Effects of endolithic parasitism on invasive and indigenous mussels in a variable physical environment. PLoS One 4(8):e6560. CrossRefPubMedPubMedCentralGoogle Scholar
  78. Zardi GI, Nicastro KR, Ferreira Costa J, Serrão EA, Pearson GA (2013) Broad scale agreement between intertidal habitats and adaptive traits on a basis of contrasting population genetic structure. Estuar Coast Shelf Sci 131:140–148CrossRefGoogle Scholar
  79. Zardi GI, Nicastro KR, McQuaid CD, Castilho R, Costa J, Serrão EA, Pearson GA (2015) Intraspecific genetic lineages of a marine mussel show behavioural divergence and spatial segregation over a tropical/subtropical biogeographic transition. BMC Evol Biol 15(100):1–11Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.South African Institute for Aquatic Biodiversity (SAIAB)GrahamstownSouth Africa
  2. 2.Nucleo Milenio, Centro de Conservación Marina and Estación Costera de Investigaciones MarinasPontificia Universidad Católica de ChileSantiagoChile
  3. 3.Departamento de Bioquímica, Genética e InmunologíaUniversidad de VigoVigoSpain
  4. 4.The Department of Zoology and EntomologyRhodes UniversityGrahamstownSouth Africa

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