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

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Cell Stress and Chaperones Aims and scope

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.

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References

  • 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 13:739–755

    Article  CAS  PubMed  Google Scholar 

  • 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 11:539–547

    Article  Google Scholar 

  • Badyaev AV (2005) Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation. Proc R Soc B 272:877–886

    Article  PubMed Central  PubMed  Google Scholar 

  • Baur B (1988) Microgeographical variation in shell size of the land snail Chondrina clienta. Biol J Linn Soc 35:247–259

    Article  Google Scholar 

  • Baur B, Raboud C (1988) Life history of the land snail Arianta arbustorum along an altitudinal gradient. J Anim Ecol 57:71–87

    Article  Google Scholar 

  • Bettencourt BR, Feder FE, Cavicchi S (1999) Experimental evolution of Hsp70 expression and thermotolerance in Drosophila melanogaster. Evolution 53:484–492

    Article  CAS  Google Scholar 

  • Bolker J (2012) There’s more to life than rats and flies. Nature 491:31–33

    Article  CAS  PubMed  Google Scholar 

  • 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 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Bukau B, Horwich AL (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92:351–366

    Article  CAS  PubMed  Google Scholar 

  • Child GP, Blanc R, Plough HH (1940) Somatic effects of temperature on development in Drosophila melanogaster. Physiol Zool 13:56–64

    Google Scholar 

  • Cowie RH (1984) Ecogenetics of Theba pisana (Pulmonata: Helicidae) at the northern edge of its range. Malacology 25:361–380

    Google Scholar 

  • Cowie RH (1990) Climatic selection on body colour in the land snail Theba pisana (Pulmonata: Helicidae). Heredity 65:123–126

    Article  Google Scholar 

  • Cowie RH, Cain AJ (1983) Laboratory maintenance and breeding of land snails, with an example of Helix aspersa. J Molluscan Stud 49:176–179

    Google Scholar 

  • Crichigno SA, Battini MA, Cussac VE (2012) Early morphological variation and induction of phenotypic plasticity in Patagonian pejerrey. Neotropical Ichthyol 10:341–348

    Article  Google Scholar 

  • 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 12:786–793

    Article  Google Scholar 

  • 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 17:717–727

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 18:405–414

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dusheck J (2002) It’s the ecology, stupid! Nature 418:578–579

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin vers. 3.0: an integrated software package for population genetics data analysis. Evol Bioinformatics Online 1:47–50

    CAS  Google Scholar 

  • Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282

    Article  CAS  PubMed  Google Scholar 

  • 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 3:294–299

    CAS  PubMed  Google Scholar 

  • Gething M-J, Sambrook J (1992) Protein folding in the cell. Nature 355:33–45

    Article  CAS  PubMed  Google Scholar 

  • Haap T, Köhler H-R (2009) Cadmium tolerance in seven Daphnia magna clones is associated with reduced hsp70 baseline levels and induction. Aquat Toxicol 94:131–137

    Article  CAS  PubMed  Google Scholar 

  • Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • 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 10:689–696

    Article  Google Scholar 

  • Helmus MR, Bland TJ, Williams CK, Ives AR (2007) Phylogenetic measures of biodiversity. Am Nat 169:E68–E83

    Article  PubMed  Google Scholar 

  • Horn HS (1966) Measurement of “overlap” in comparative ecological studies. Am Nat 100:419–424

    Article  Google Scholar 

  • 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 285:13254–13263

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 61:117–126

    Google Scholar 

  • 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 350:133–141

    Article  CAS  PubMed  Google Scholar 

  • Johnson MS (1981) Effects of migration and habitat choice on shell banding frequencies in Theba pisana at a habitat boundary. Heredity 47:121–133

    Article  Google Scholar 

  • Johnson MS (2011) Thirty-four years of climatic selection in the land snail Theba pisana. Heredity 106:741–748

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Johnson MS (2012) Epistasis, phenotypic disequilibrium and contrasting associations with climate in the land snail Theba pisana. Heredity 108:229–235

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    Article  CAS  PubMed  Google Scholar 

  • Jones JS, Selander RK, Schnell GD (1982) Patterns of morphological and molecular polymorphism in the land snail Cepaea nemoralis. Biol J Linn Soc 14:359–387

    Article  Google Scholar 

  • 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 42:341–362

    Article  CAS  Google Scholar 

  • 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 71:221–231

    Article  Google Scholar 

  • 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 22:334–338

    PubMed  Google Scholar 

  • 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 11:43–52

    Article  Google Scholar 

  • Köhler H-R, Zanger M, Eckwert H, Einfeldt I (2000) Selection favours low Hsp70 levels in chronically metal-stressed soil arthropods. J Evol Biol 13:569–582

    Article  Google Scholar 

  • 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 141:398–405

    Google Scholar 

  • 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:136–147

    Article  Google Scholar 

  • 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 119:241–256

    Article  Google Scholar 

  • Krebs RA, Feder ME (1997) Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larvae. Cell Stress Chaperones 2:60–71

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Krebs RA, Loeschcke V (1994) Costs and benefits of activation of the heat shock response in Drosophila melanogaster. Funct Ecol 8:730–737

    Article  Google Scholar 

  • 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 105:216–221

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 8:351–368

    Article  CAS  Google Scholar 

  • Lindquist S, Craig EA (1988) The heat shock proteins. Ann Rev Genet 22:631–677

    Article  CAS  PubMed  Google Scholar 

  • Machin J (1968) The permeability of the epiphragm of terrestrial snails to water vapor. Biol Bull Mar Biol Lab Woods Hole 134:87–95

    Article  Google Scholar 

  • 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 30:1–11

    Article  CAS  PubMed  Google Scholar 

  • Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62:670–684

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mazek-Fialla K (1934) Die Lebensweise xerophiler Schnecken Syriens, Griechlands, Dalmatiens und der Türkei und die Beschaffenheit ihrer subepithelialen Drüsen. Z Morphol Okol Tiere 28:445–468

    Article  Google Scholar 

  • Mizrahi T, Heller J, Goldenberg S, Arad Z (2009) Heat shock proteins and resistance to desiccation in congeneric land snails. Cell Stress Chaperones 15:351–363

    Article  PubMed Central  PubMed  Google Scholar 

  • Müller GB (2003) Embryonic motility: environmental influences and evolutionary innovation. Evol Dev 5:56–60

    Article  PubMed  Google Scholar 

  • Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci U S A 70:3321–3323

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 231–244

  • 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

  • Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27:437–496

    Article  CAS  PubMed  Google Scholar 

  • Pörtner HO, Farrell AP (2008) Ecology: physiology and climate change. Science 322:690–692

    Article  PubMed  Google Scholar 

  • Price TD, Qvarnström A, Irwin DE (2003) The role of phenotypic plasticity in driving genetic evolution. Proc R Soc Lond B 270:1433–1440

    Article  Google Scholar 

  • Queitsch C, Sangster TA, Lindquist S (2002) Hsp90 as a capacitor of phenotypic variation. Nature 417:618–624

    Article  CAS  PubMed  Google Scholar 

  • 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

  • Rebeiz M, Pool JE, Kassner VA, Aquadro CF, Carroll SB (2009) Stepwise modification of a modular enhancer underlies adaptation in a Drosophila population. Science 326:1663–1667

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Roberts SP, Feder ME (1999) Natural hyperthermia and expression of the heat shock protein Hsp70 affect developmental abnormalities in Drosophila melanogaster. Oecologia 121:323–329

    Article  Google Scholar 

  • Rosseel Y (2012) lavaan: An R package for structural equation modeling. J Stat Softw 48:1--16

    Google Scholar 

  • Royer DL, Meyerson LA, Robertson KM, Adams JM (2009) Phenotypic plasticity of leaf shape along a temperature gradient in Acer rubrum. PLoS ONE 4:e7653

    Article  PubMed Central  PubMed  Google Scholar 

  • Rutherford SL (2003) Between genotype and phenotype: protein chaperones and evolvability. Nat Rev Genet 4:263–274

    Article  CAS  PubMed  Google Scholar 

  • Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396:336–342

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Silbermann R, Tatar M (2000) Reproduction costs of heat shock protein in transgenic Drosophila melanogaster. Evolution 54:2038–2045

    Article  CAS  PubMed  Google Scholar 

  • Sisodia S, Singh BN (2009) Variations in morphological and life-history traits under extreme temperatures in Drosophila ananassae. J Biosci 34:263–274

    Article  PubMed  Google Scholar 

  • 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 131:155–164

    Article  PubMed  Google Scholar 

  • 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 15:289–296

    Article  Google Scholar 

  • Sultan SE (2007) Development in context: the timely emergence of eco-devo. Trends Ecol Evol 22:575–582

    Article  PubMed  Google Scholar 

  • Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150:563–565

    Article  Google Scholar 

  • Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J R Stat Soc B 73(1):3–36

    Article  Google Scholar 

  • 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 204:1869–1881

    CAS  PubMed  Google Scholar 

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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).

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Authors and Affiliations

  1. Animal Physiological Ecology, Institute of Evolution and Ecology, Tübingen University, Konrad-Adenauer-Str. 20, D-72072, Tübingen, Germany

    Maddalena A. Di Lellis, Anna Geißler, Petra Arnold, Stefanie Lang, Sandra Troschinski, Andreas Dieterich, Stefanie Krais, Rita Triebskorn & Heinz-R. Köhler

  2. Department of Animal Ecology & Systematics, Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32 IFZ, D-35392, Giessen, Germany

    Sergej Sereda, Torsten Hauffe & Thomas Wilke

  3. Laboratory of Ecotoxicology (LEMA), EA 3222 PRES Normandie, Le Havre University, 25 Rue Philippe Lebon, F-76058, Le Havre Cedex, France

    Adrien Picot, Thomas Knigge & Tiphaine Monsinjon

  4. Université d’Avignon et des Pays de Vaucluse, Laboratoire de Toxicologie Environnementale, UMR 406 UAPV/INRA, Domaine St Paul, Site Agroparc, F-84914, Avignon Cedex 9, France

    Yvan Capowiez

  5. IMBE UMR 7263, Institut Mediterranéen de Biodiversité et d’Ecologie marine et continentale, Université d’Avignon et des Pays de Vaucluse, Pole Agrosciences, 301 rue Baruch de Spinoza, BP 21239, F-84916, Avignon cedex 9, France

    Christophe Mazzia

  6. Steinbeis-Transfer Center Ecotoxicology and Ecophysiology Rottenburg, Blumenstr. 13, D-72108, Rottenburg, Germany

    Rita Triebskorn

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  1. Maddalena A. Di Lellis
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  2. Sergej Sereda
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Correspondence to Maddalena A. Di Lellis or Heinz-R. Köhler.

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Di Lellis, M.A., Sereda, S., Geißler, A. et al. Phenotypic diversity, population structure and stress protein-based capacitoring in populations of Xeropicta derbentina, a heat-tolerant land snail species. Cell Stress and Chaperones 19, 791–800 (2014). https://doi.org/10.1007/s12192-014-0503-x

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