Advertisement

Cell Stress and Chaperones

, Volume 19, Issue 6, pp 791–800 | Cite as

Phenotypic diversity, population structure and stress protein-based capacitoring in populations of Xeropicta derbentina, a heat-tolerant land snail species

  • Maddalena A. Di LellisEmail author
  • Sergej Sereda
  • Anna Geißler
  • Adrien Picot
  • Petra Arnold
  • Stefanie Lang
  • Sandra Troschinski
  • Andreas Dieterich
  • Torsten Hauffe
  • Yvan Capowiez
  • Christophe Mazzia
  • Thomas Knigge
  • Tiphaine Monsinjon
  • Stefanie Krais
  • Thomas Wilke
  • Rita Triebskorn
  • Heinz-R. KöhlerEmail author
Original Paper

Abstract

The shell colour of many pulmonate land snail species is highly diverse. Besides a genetic basis, environmentally triggered epigenetic mechanisms including stress proteins as evolutionary capacitors are thought to influence such phenotypic diversity. In this study, we investigated the relationship of stress protein (Hsp70) levels with temperature stress tolerance, population structure and phenotypic diversity within and among different populations of a xerophilic Mediterranean snail species (Xeropicta derbentina). Hsp70 levels varied considerably among populations, and were significantly associated with shell colour diversity: individuals in populations exhibiting low diversity expressed higher Hsp70 levels both constitutively and under heat stress than those of phenotypically diverse populations. In contrast, population structure (cytochrome c oxidase subunit I gene) did not correlate with phenotypic diversity. However, genetic parameters (both within and among population differences) were able to explain variation in Hsp70 induction at elevated but non-pathologic temperatures. Our observation that (1) population structure had a high explanatory potential for Hsp70 induction and that (2) Hsp70 levels, in turn, correlated with phenotypic diversity while (3) population structure and phenotypic diversity failed to correlate provides empirical evidence for Hsp70 to act as a mediator between genotypic variation and phenotype and thus for chaperone-driven evolutionary capacitance in natural populations.

Keywords

COI Eco-devo Evolutionary capacitance Hsp70 Xeropicta derbentina 

Notes

Acknowledgments

We are grateful to Tim Triebskorn, Nik Triebskorn, and Thierry Desmarest for their help with the field work. François Leboulenger provided valuable information on the distribution of land snails in France. This study was financed by the German Research Council, DFG (KO 1978/5-3 and WI 1902/10-3).

References

  1. Arts M-JSJ, Schill RO, Knigge T, Eckwert H, Kammenga JE, Köhler H-R (2004) Stress proteins (hsp70, hsp60) induced in isopods and nematodes by field exposure to metals in a gradient near Avonmouth, UK. Ecotoxicology 13:739–755PubMedCrossRefGoogle Scholar
  2. Aubry S, Labaune C, Magnin F, Kiss L (2005) Habitat and integration within indigenous communities of Xeropicta derbentina (Gastropoda: Hygromiidae), a recently introduced land snail in South-Eastern France. Divers Distrib 11:539–547CrossRefGoogle Scholar
  3. Badyaev AV (2005) Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation. Proc R Soc B 272:877–886PubMedCentralPubMedCrossRefGoogle Scholar
  4. Baur B (1988) Microgeographical variation in shell size of the land snail Chondrina clienta. Biol J Linn Soc 35:247–259CrossRefGoogle Scholar
  5. Baur B, Raboud C (1988) Life history of the land snail Arianta arbustorum along an altitudinal gradient. J Anim Ecol 57:71–87CrossRefGoogle Scholar
  6. Bettencourt BR, Feder FE, Cavicchi S (1999) Experimental evolution of Hsp70 expression and thermotolerance in Drosophila melanogaster. Evolution 53:484–492CrossRefGoogle Scholar
  7. Bolker J (2012) There’s more to life than rats and flies. Nature 491:31–33PubMedCrossRefGoogle Scholar
  8. Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principles of protein-dye binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  9. Bukau B, Horwich AL (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92:351–366PubMedCrossRefGoogle Scholar
  10. Child GP, Blanc R, Plough HH (1940) Somatic effects of temperature on development in Drosophila melanogaster. Physiol Zool 13:56–64Google Scholar
  11. Cowie RH (1984) Ecogenetics of Theba pisana (Pulmonata: Helicidae) at the northern edge of its range. Malacology 25:361–380Google Scholar
  12. Cowie RH (1990) Climatic selection on body colour in the land snail Theba pisana (Pulmonata: Helicidae). Heredity 65:123–126CrossRefGoogle Scholar
  13. Cowie RH, Cain AJ (1983) Laboratory maintenance and breeding of land snails, with an example of Helix aspersa. J Molluscan Stud 49:176–179Google Scholar
  14. Crichigno SA, Battini MA, Cussac VE (2012) Early morphological variation and induction of phenotypic plasticity in Patagonian pejerrey. Neotropical Ichthyol 10:341–348CrossRefGoogle Scholar
  15. Dahlgaard J, Loeschcke V, Michalak P, Justesen J (1998) Induced thermotolerance and associated expression of the heat shock protein Hsp70 in adult Drosophila melanogaster. Funct Ecol 12:786–793CrossRefGoogle Scholar
  16. Di Lellis MA, Seifan M, Troschinski S, Mazzia C, Capowiez Y, Triebskorn R, Köhler H-R (2012) Solar radiation stress in climbing snails: behavioural and intrinsic features define the Hsp70 level in natural populations of Xeropicta derbentina (Pulmonata). Cell Stress Chaperones 17:717–727PubMedCentralPubMedCrossRefGoogle Scholar
  17. Dieterich A, Fischbach U, Ludwig M, Di Lellis MA, Troschinski S, Gärtner U, Triebskorn R, Köhler H-R (2013) Daily and seasonal changes in heat exposure and the Hsp70 level of individuals from a field population of Xeropicta derbentina (Krynicki 1836) (Pulmonata, Hygromiidae) in Southern France. Cell Stress Chaperones 18:405–414PubMedCentralPubMedCrossRefGoogle Scholar
  18. Dusheck J (2002) It’s the ecology, stupid! Nature 418:578–579PubMedCrossRefGoogle Scholar
  19. Excoffier L, Laval G, Schneider S (2005) Arlequin vers. 3.0: an integrated software package for population genetics data analysis. Evol Bioinformatics Online 1:47–50Google Scholar
  20. Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282PubMedCrossRefGoogle Scholar
  21. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299PubMedGoogle Scholar
  22. Gething M-J, Sambrook J (1992) Protein folding in the cell. Nature 355:33–45PubMedCrossRefGoogle Scholar
  23. Haap T, Köhler H-R (2009) Cadmium tolerance in seven Daphnia magna clones is associated with reduced hsp70 baseline levels and induction. Aquat Toxicol 94:131–137PubMedCrossRefGoogle Scholar
  24. Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  25. Hansen LR, Soylu S, Kotaki Y, Moestrup Ø, Lundholm N (2011) Toxin production and temperature-induced morphological variation of the diatom Pseudo-nitzschia seriata from the Arctic. Harmful Algae 10:689–696CrossRefGoogle Scholar
  26. Helmus MR, Bland TJ, Williams CK, Ives AR (2007) Phylogenetic measures of biodiversity. Am Nat 169:E68–E83PubMedCrossRefGoogle Scholar
  27. Horn HS (1966) Measurement of “overlap” in comparative ecological studies. Am Nat 100:419–424CrossRefGoogle Scholar
  28. Hoshino T, Matsuda M, Yamashita Y, Takehara M, Fukuya M, Mineda K, Maji D, Ihn H, Adachi H, Sobue G, Funasaka Y, Mizushima T (2010) Suppression of melanin production by expression of Hsp70. J Biol Chem 285:13254–13263PubMedCentralPubMedCrossRefGoogle Scholar
  29. Imasheva AG, Loeschcke V, Zhivotovsky LA, Lazebny OE (1997) Effect of extreme temperatures on phenotypic variation and developmental stability in Drosophila melanogaster and Drosophila buzzatii. Biol J Linn Soc 61:117–126Google Scholar
  30. Jablonka E, Oborny B, Molnar I, Kisdi E, Hofbauer J, Czaran T (1995) The adaptive advantage of phenotypic memory in changing environments. Phil Trans R Soc B 350:133–141PubMedCrossRefGoogle Scholar
  31. Johnson MS (1981) Effects of migration and habitat choice on shell banding frequencies in Theba pisana at a habitat boundary. Heredity 47:121–133CrossRefGoogle Scholar
  32. Johnson MS (2011) Thirty-four years of climatic selection in the land snail Theba pisana. Heredity 106:741–748PubMedCentralPubMedCrossRefGoogle Scholar
  33. Johnson MS (2012) Epistasis, phenotypic disequilibrium and contrasting associations with climate in the land snail Theba pisana. Heredity 108:229–235PubMedCentralPubMedCrossRefGoogle Scholar
  34. Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405PubMedCrossRefGoogle Scholar
  35. Jones JS, Selander RK, Schnell GD (1982) Patterns of morphological and molecular polymorphism in the land snail Cepaea nemoralis. Biol J Linn Soc 14:359–387CrossRefGoogle Scholar
  36. Kartavtsev YP, Lee JS (2006) Analysis of nucleotide diversity at the cytochrome b and cytochrome oxidase 1 genes at the population, species, and genus levels. Russ J Genet 42:341–362CrossRefGoogle Scholar
  37. Kiss L, Labaune C, Magnin F, Aubry S (2005) Plasticity of the life cycle of Xeropicta derbentina (Krynicki, 1836), a recently introduced snail in Mediterranean France. J Molluscan Stud 71:221–231CrossRefGoogle Scholar
  38. Köhler H-R, Triebskorn R, Stöcker W, Kloetzel PM, Alberti G (1992) The 70kD heat shock protein (Hsp 70) in soil invertebrates: a possible tool for monitoring environmental toxicants. Arch Environ Contam Toxicol 22:334–338PubMedGoogle Scholar
  39. Köhler H-R, Eckwert H, Triebskorn R, Bengtsson G (1999) Interaction between tolerance and 70 kD stress protein (Hsp70) induction in collembolan populations exposed to long-term metal pollution. Appl Soil Ecol 11:43–52CrossRefGoogle Scholar
  40. Köhler H-R, Zanger M, Eckwert H, Einfeldt I (2000) Selection favours low Hsp70 levels in chronically metal-stressed soil arthropods. J Evol Biol 13:569–582CrossRefGoogle Scholar
  41. Köhler H-R, Alberti G, Seniczak S, Seniczak A (2005) Lead-induced hsp70 and hsp60 pattern transformation and leg malformation during postembryonic development in the oribatid mite, Archegozetes longisetosus Aoki. Comp Biochem Physiol C 141:398–405Google Scholar
  42. Köhler H-R, Lazzara R, Dittbrenner N, Capowiez Y, Mazzia C, Triebskorn R (2009) Snail phenotypic variation and stress proteins: do different heat response strategies contribute to Waddington’s Widget in field populations? J Exp Zool B Mol Dev Evol 312B:136–147CrossRefGoogle Scholar
  43. Köhler H-R, Schultz C, Scheil AE, Triebskorn R, Seifan M, Di Lellis MA (2013) Historic data analysis reveals ambient temperature as a source of phenotypic variation in snail populations. Biol J Linn Soc 119:241–256CrossRefGoogle Scholar
  44. Krebs RA, Feder ME (1997) Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larvae. Cell Stress Chaperones 2:60–71PubMedCentralPubMedCrossRefGoogle Scholar
  45. Krebs RA, Loeschcke V (1994) Costs and benefits of activation of the heat shock response in Drosophila melanogaster. Funct Ecol 8:730–737CrossRefGoogle Scholar
  46. Kristensen TN, Hoffmann AA, Overgaard J, Sorensen JG, Hallas R, Loeschcke V (2008) Costs and benefits of cold acclimation in field-released Drosophila. Proc Natl Acad Sci U S A 105:216–221PubMedCentralPubMedCrossRefGoogle Scholar
  47. Lewis S, Handy RD, Cordi B, Billinghurst Z, Depledge MH (1999) Stress proteins (Hsps): methods of detection and their use as an environmental biomarker. Ecotoxicology 8:351–368CrossRefGoogle Scholar
  48. Lindquist S, Craig EA (1988) The heat shock proteins. Ann Rev Genet 22:631–677PubMedCrossRefGoogle Scholar
  49. Machin J (1968) The permeability of the epiphragm of terrestrial snails to water vapor. Biol Bull Mar Biol Lab Woods Hole 134:87–95CrossRefGoogle Scholar
  50. Manitasevic S, Dunderski J, Matic G, Tucic B (2007) Seasonal variation in heat shock proteins Hsp70 and Hsp90 expression in an exposed and a shaded habitat of Iris pumila. Plant Cell Environ 30:1–11PubMedCrossRefGoogle Scholar
  51. Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62:670–684PubMedCentralPubMedCrossRefGoogle Scholar
  52. Mazek-Fialla K (1934) Die Lebensweise xerophiler Schnecken Syriens, Griechlands, Dalmatiens und der Türkei und die Beschaffenheit ihrer subepithelialen Drüsen. Z Morphol Okol Tiere 28:445–468CrossRefGoogle Scholar
  53. Mizrahi T, Heller J, Goldenberg S, Arad Z (2009) Heat shock proteins and resistance to desiccation in congeneric land snails. Cell Stress Chaperones 15:351–363PubMedCentralPubMedCrossRefGoogle Scholar
  54. Müller GB (2003) Embryonic motility: environmental influences and evolutionary innovation. Evol Dev 5:56–60PubMedCrossRefGoogle Scholar
  55. Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci U S A 70:3321–3323PubMedCentralPubMedCrossRefGoogle Scholar
  56. Norris CE & Hightower LE (2000) The heat shock response of tropical and desert fish (genus Poeciliopsis). Environmental Stressors and Gene Responses. In: Storey KB & Storey JM (Eds) Elsevier Science, Series: Cell and Molecular Responses to Stress, pp 231–244Google Scholar
  57. Oksanen J, Guillaume Blanchet F, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H & Wagner H (2012) vegan: Community Ecology Package R package version 2.0-5 http://CRAN.R-project.org/package=vegan
  58. Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27:437–496PubMedCrossRefGoogle Scholar
  59. Pörtner HO, Farrell AP (2008) Ecology: physiology and climate change. Science 322:690–692PubMedCrossRefGoogle Scholar
  60. Price TD, Qvarnström A, Irwin DE (2003) The role of phenotypic plasticity in driving genetic evolution. Proc R Soc Lond B 270:1433–1440CrossRefGoogle Scholar
  61. Queitsch C, Sangster TA, Lindquist S (2002) Hsp90 as a capacitor of phenotypic variation. Nature 417:618–624PubMedCrossRefGoogle Scholar
  62. R Development Core Team (2011) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0 http://www.R-project.org
  63. Rebeiz M, Pool JE, Kassner VA, Aquadro CF, Carroll SB (2009) Stepwise modification of a modular enhancer underlies adaptation in a Drosophila population. Science 326:1663–1667PubMedCentralPubMedCrossRefGoogle Scholar
  64. Roberts SP, Feder ME (1999) Natural hyperthermia and expression of the heat shock protein Hsp70 affect developmental abnormalities in Drosophila melanogaster. Oecologia 121:323–329CrossRefGoogle Scholar
  65. Rosseel Y (2012) lavaan: An R package for structural equation modeling. J Stat Softw 48:1--16Google Scholar
  66. Royer DL, Meyerson LA, Robertson KM, Adams JM (2009) Phenotypic plasticity of leaf shape along a temperature gradient in Acer rubrum. PLoS ONE 4:e7653PubMedCentralPubMedCrossRefGoogle Scholar
  67. Rutherford SL (2003) Between genotype and phenotype: protein chaperones and evolvability. Nat Rev Genet 4:263–274PubMedCrossRefGoogle Scholar
  68. Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396:336–342PubMedCrossRefGoogle Scholar
  69. Schrader M, Hauffe T, Zhang Z, Davis GM, Jopp F, Remais JV, Wilke T (2013) Spatially explicit modeling of schistosomiasis risk in Eastern China based on a synthesis of epidemiological, environmental and intermediate host genetic data. PLoS Negl Trop Dis 7:e2327. doi: 10.1371/journal.pntd.0002327 PubMedCentralPubMedCrossRefGoogle Scholar
  70. Silbermann R, Tatar M (2000) Reproduction costs of heat shock protein in transgenic Drosophila melanogaster. Evolution 54:2038–2045PubMedCrossRefGoogle Scholar
  71. Sisodia S, Singh BN (2009) Variations in morphological and life-history traits under extreme temperatures in Drosophila ananassae. J Biosci 34:263–274PubMedCrossRefGoogle Scholar
  72. Sørensen JG, Michalak P, Justesen J, Loeschcke V (1999) Expression of the heat shock protein HSP70 in Drosophila buzzatii lines selected for thermal resistance traits. Hereditas 131:155–164PubMedCrossRefGoogle Scholar
  73. Sørensen JG, Dahlgaard J, Loeschcke V (2001) Genetic variation in thermal tolerance among natural populations of Drosophila buzzatii: down regulation of Hsp70 expression and variation in heat stress resistance traits. Funct Ecol 15:289–296CrossRefGoogle Scholar
  74. Sultan SE (2007) Development in context: the timely emergence of eco-devo. Trends Ecol Evol 22:575–582PubMedCrossRefGoogle Scholar
  75. Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150:563–565CrossRefGoogle Scholar
  76. Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J R Stat Soc B 73(1):3–36CrossRefGoogle Scholar
  77. Zatsepina OG, Velikodvorskaia VV, Molodtsov VB, Garbuz D, Lerman DN, Bettencourt BR, Feder ME, Evgenev MB (2001) A Drosophila melanogaster strain from sub-equatorial Africa has exceptional thermotolerance but decreased Hsp70 expression. J Exp Biol 204:1869–1881PubMedGoogle Scholar

Copyright information

© Cell Stress Society International 2014

Authors and Affiliations

  • Maddalena A. Di Lellis
    • 1
    Email author
  • Sergej Sereda
    • 2
  • Anna Geißler
    • 1
  • Adrien Picot
    • 3
  • Petra Arnold
    • 1
  • Stefanie Lang
    • 1
  • Sandra Troschinski
    • 1
  • Andreas Dieterich
    • 1
  • Torsten Hauffe
    • 2
  • Yvan Capowiez
    • 4
  • Christophe Mazzia
    • 5
  • Thomas Knigge
    • 3
  • Tiphaine Monsinjon
    • 3
  • Stefanie Krais
    • 1
  • Thomas Wilke
    • 2
  • Rita Triebskorn
    • 1
    • 6
  • Heinz-R. Köhler
    • 1
    Email author
  1. 1.Animal Physiological Ecology, Institute of Evolution and EcologyTübingen UniversityTübingenGermany
  2. 2.Department of Animal Ecology & SystematicsJustus Liebig University GiessenGiessenGermany
  3. 3.Laboratory of Ecotoxicology (LEMA), EA 3222 PRES NormandieLe Havre UniversityLe Havre CedexFrance
  4. 4.Université d’Avignon et des Pays de Vaucluse, Laboratoire de Toxicologie Environnementale, UMR 406 UAPV/INRAAvignon Cedex 9France
  5. 5.IMBE UMR 7263, Institut Mediterranéen de Biodiversité et d’Ecologie marine et continentaleUniversité d’Avignon et des Pays de Vaucluse, Pole AgrosciencesAvignon cedex 9France
  6. 6.Steinbeis-Transfer Center Ecotoxicology and Ecophysiology RottenburgRottenburgGermany

Personalised recommendations