Behavioral Ecology and Sociobiology

, Volume 67, Issue 4, pp 649–656 | Cite as

Pathogen-induced hatching and population-specific life-history response to waterborne cues in brown trout (Salmo trutta)

Original Paper

Abstract

Hatching is an important niche shift, and embryos in a wide range of taxa can either accelerate or delay this life-history switch in order to avoid stage-specific risks. Such behavior can occur in response to stress itself and to chemical cues that allow anticipation of stress. We studied the genetic organization of this phenotypic plasticity and tested whether there are differences among populations and across environments in order to learn more about the evolutionary potential of stress-induced hatching. As a study species, we chose the brown trout (Salmo trutta; Salmonidae). Gametes were collected from five natural populations (within one river network) and used for full-factorial in vitro fertilizations. The resulting embryos were either directly infected with Pseudomonas fluorescens or were exposed to waterborne cues from P. fluorescens-infected conspecifics. We found that direct inoculation with P. fluorescens increased embryonic mortality and induced hatching in all host populations. Exposure to waterborne cues revealed population-specific responses. We found significant additive genetic variation for hatching time, and genetic variation in trait plasticity. In conclusion, hatching is induced in response to infection and can be affected by waterborne cues of infection, but populations and families differ in their reaction to the latter.

Keywords

Additive genetic variation Fish embryo Induced hatching Niche shift Phenotypic plasticity Reaction norm Salmonid 

Notes

Acknowledgments

We thank the members of the Fisheries Inspectorate Bern for their support, and especially U. Gutmann, J. Gutruf, C. Küng, M. Schmid, and H. Walther for permissions, for catching and taking care of the adult fish, and for assistance during the preparations of the in vitro fertilizations. Thanks also to G. Brazzola, P. Christe, M. dos Santos, S. Einum, N. Perrin, A. Ross-Gillespie, R. Stelkens, C. van Oosterhout, and L. Wilkins for help in the field and/or useful discussions, T. Bakker, K. Warkentin and two reviewers for comments on the manuscript, and the Swiss National Science Foundation and the Foundation Maison de la Rivière for financial support.

Ethical standards

Permissions for handling embryos were granted by the local authority (i.e., the Fishery Inspectorate of the Bern canton). The manipulations of the adults were part of the yearly hatchery program of the Bern canton. Experimental manipulations on embryos were performed prior to yolk sac absorption. All manipulations comply with the current law of the country in which they were performed (Switzerland).

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Agrawal A, Conner J, Johnson M, Wallsgrove R (2002) Ecological genetics of an induced plant defense against herbivores: additive genetic variance and costs of phenotypic plasticity. Evolution 56:2206–2213PubMedGoogle Scholar
  2. Anderson AL, Brown WD (2009) Plasticity of hatching in green frogs (Rana clamitans) to both egg and tadpole predators. Herpetologica 65:207–213CrossRefGoogle Scholar
  3. Austin B, Austin DA (2007) Bacterial fish pathogens: disease of farmed and wild fish, 4th edn. Springer Praxis, Chichester, UKGoogle Scholar
  4. Bates D, Sarkar D (2007) lme4: linear mixed-effects models using S4 classes (R package); http://cran.r-project.org/web/packages/lme4
  5. Chivers DP, Kiesecker JM, Marco A, De Vito J, Anderson MT, Blaustein AR (2001) Predator-induced life history changes in amphibians: egg predation induces hatching. Oikos 92:135–142CrossRefGoogle Scholar
  6. Crozier LG, Hendry AP, Lawson PW, Quinn TP, Mantua NJ, Battin J, Shaw RG, Huey RB (2008) Potential responses to climate change in organisms with complex life histories: evolution and plasticity in Pacific salmon. Evol Appl 1:252–270CrossRefGoogle Scholar
  7. Dewitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81PubMedCrossRefGoogle Scholar
  8. Dobson A, Foufopoulos J (2001) Emerging infectious pathogens of wildlife. Philos T Roy Soc B 356:1001–1012CrossRefGoogle Scholar
  9. Einum S, Fleming I (2000) Selection against late emergence and small offspring in Atlantic salmon (Salmo salar). Evolution 54:628–639PubMedGoogle Scholar
  10. Evans ML, Neff BD (2009) Major histocompatibility complex heterozygote advantage and widespread bacterial infections in populations of Chinook salmon (Oncorhynchus tshawytscha). Mol Ecol 18:4716–4729PubMedCrossRefGoogle Scholar
  11. Evans ML, Neff BD, Heath DD (2010) Quantitative genetic and translocation experiments reveal genotype-by-environment effects on juvenile life-history traits in two populations of Chinook salmon (Oncorhynchus tshawytscha). J Evol Biol 23:687–698PubMedCrossRefGoogle Scholar
  12. Fisher RA (1930) The genetical theory of natural selection. Clarendon, Oxford, EnglandGoogle Scholar
  13. Gomez-Mestre I, Touchon JC, Saccoccio VL, Warkentin KM (2008) Genetic variation in pathogen-induced early hatching of toad embryos. J Evol Biol 21:791–800PubMedCrossRefGoogle Scholar
  14. Gomez-Mestre I, Touchon JC, Warkentin KM (2006) Amphibian embryo and parental defenses and a larval predator reduce egg mortality from water mold. Ecology 87:2570–2581PubMedCrossRefGoogle Scholar
  15. Gomez-Mestre I, Warkentin KM (2007) To hatch and hatch not: similar selective trade-offs but different responses to egg predators in two closely related, syntopic treefrogs. Oecologia 153:197–206PubMedCrossRefGoogle Scholar
  16. Harvell CD (1999) Emerging marine diseases—climate links and anthropogenic factors. Science 285:1505–1510PubMedCrossRefGoogle Scholar
  17. Hoffmann A, Merilä J (1999) Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol Evol 14:96–101PubMedCrossRefGoogle Scholar
  18. Holt JA, Krieg NR, Sneath PHA, Staley JT, Williams ST (1994) Bergey’s manual of determinative bacteriology, 9th edn. Williams & Wilkins, Baltimore, USA, p 5Google Scholar
  19. Houle D (1992) Comparing evolvability and variability of quantitative traits. Genetics 130:195–204PubMedGoogle Scholar
  20. Hutchings JA (2011) Old wine in new bottles: reaction norms in salmonid fishes. Heredity 106:421–437PubMedCrossRefGoogle Scholar
  21. Jacob A, Evanno G, von Siebenthal BA, Grossen C, Wedekind C (2010) Effects of different mating scenarios on embryo viability in brown trout. Mol Ecol 19:5296–5307PubMedCrossRefGoogle Scholar
  22. Jacob A, Nusslé S, Britschgi A, Evanno G, Müller R, Wedekind C (2007) Male dominance linked to size and age, but not to ‘good genes’ in brown trout (Salmo trutta). BMC Evol Biol 7:207PubMedCrossRefGoogle Scholar
  23. Jensen LF, Hansen MM, Pertoldi C, Holdensgaard G, Mensberg K-LD, Loeschcke V (2008) Local adaptation in brown trout early life-history traits: implications for climate change adaptability. Proc R Soc Lond B 275:2859–2868CrossRefGoogle Scholar
  24. JMP V (1989–2007) SAS Institute Inc., Cary, NCGoogle Scholar
  25. Johnson PTJ, Kellermanns E, Bowerman J (2011) Critical windows of disease risk: amphibian pathology driven by developmental changes in host resistance and tolerance. Funct Ecol 25:726–734CrossRefGoogle Scholar
  26. Kearsey M, Pooni H (1996) The genetical analyses of quantitative traits. Chapman and Hall, LondonGoogle Scholar
  27. Kiesecker J, Skelly D, Beard K, Preisser E (1999) Behavioral reduction of infection risk. P Natl Acad Sci USA 96:9165–9168CrossRefGoogle Scholar
  28. Kraft P, Wilson R, Franklin C, Blows M (2006) Substantial changes in the genetic basis of tadpole morphology of Rana lessonae in the presence of predators. J Evol Biol 19:1813–1818PubMedCrossRefGoogle Scholar
  29. Kusch RC, Chivers DP (2004) The effects of crayfish predation on phenotypic and life-history variation in fathead minnows. Can J Zool 82:917–921CrossRefGoogle Scholar
  30. Laugen AT, Kruuk LEB, Laurila A, Rasanen K, Stone J, Merilä J (2005) Quantitative genetics of larval life-history traits in Rana temporaria in different environmental conditions. Genet Res 86:161–170PubMedCrossRefGoogle Scholar
  31. Laurila A, Karttunen S, Merilä J (2002) Adaptive phenotypic plasticity and genetics of larval life histories in two Rana temporaria populations. Evolution 56:617–627PubMedGoogle Scholar
  32. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates Inc, Sunderland, MassachusettsGoogle Scholar
  33. Martin KLM (1999) Ready and waiting: delayed hatching and extended incubation of anamniotic vertebrate terrestrial eggs. Integr Comp Biol 39:279CrossRefGoogle Scholar
  34. Merilä J (1997) Expression of genetic variation in body size of the collared flycatcher under different environmental conditions. Evolution 51:526–536CrossRefGoogle Scholar
  35. Merilä J, Fry JD (1998) Genetic variation and causes of genotype-environment interaction in the body size of blue tit (Parus caeruleus). Genetics 148:1233–1244PubMedGoogle Scholar
  36. Merilä J, Sheldon BC (1999) Genetic architecture of fitness and nonfitness traits: empirical patterns and development of ideas. Heredity 83:103–109PubMedCrossRefGoogle Scholar
  37. Merilä J, Söderman F, O’Hara R, Räsänen K, Laurila A (2004) Local adaptation and genetics of acid-stress tolerance in the moor frog, Rana arvalis. Conserv Genet 5:513–527CrossRefGoogle Scholar
  38. Miner BG, Donovan DA, Andrews KE (2010) Should I stay or should I go: predator- and conspecific-induced hatching in a marine snail. Oecologia 163:69–78PubMedCrossRefGoogle Scholar
  39. Moore R, Newton B, Sih A (1996) Delayed hatching as a response of streamside salamander eggs to chemical cues from predatory sunfish. Oikos 77:331–335CrossRefGoogle Scholar
  40. Moreira PL, Barata M (2005) Egg mortality and early embryo hatching caused by fungal infection of Iberian rock lizard (Lacerta monticola) clutches. Herpetol J 15:265–272Google Scholar
  41. Mousseau TA, Roff DA (1987) Natural selection and the heritability of fitness components. Heredity 59:181–197PubMedCrossRefGoogle Scholar
  42. OECD (1992) OECD guideline for the testing of chemicals 203 (fish acute toxicity test), Annex 2. 9; http://www.oecd-ilibrary.org, Paris, France
  43. Pakkasmaa S, Merilä J, O’Hara RB (2003) Genetic and maternal effect influences on viability of common frog tadpoles under different environmental conditions. Heredity 91:117–124PubMedCrossRefGoogle Scholar
  44. Pigliucci M (2001) Phenotypic plasticity beyond nature and nurture. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  45. R Development Core Team (2006) R: a language and environment for statistical computing. In. R Foundation for Statistical Computing; http://www.R-project.org, Vienna, Austria
  46. Reed TE, Schindler DE, Waples RS (2011) Interacting effects of phenotypic plasticity and evolution on population persistence in a changing climate. Conserv Biol 25:56–63PubMedCrossRefGoogle Scholar
  47. Relyea RA (2005) The heritability of inducible defenses in tadpoles. J Evol Biol 18:856–866PubMedCrossRefGoogle Scholar
  48. Roff DA (1997) Evolutionary quantitative genetics. Chapman & Hall, LondonCrossRefGoogle Scholar
  49. Rowe L, Ludwig D (1991) Size and timing of metamorphosis in complex life cycles: time constraints and variation. Ecology 72:413–427CrossRefGoogle Scholar
  50. Sambali G, Mehrotra R (2009) Principles of microbiology. Tata McGraw Hill, Delhi, IndiaGoogle Scholar
  51. Scarpellini M, Franzetti L, Galli A (2004) Development of PCR assay to identify Pseudomonas fluorescens and its biotope. FEMS Microbiol Lett 236:257–260PubMedCrossRefGoogle Scholar
  52. Schalk G, Forbes M, Weatherhead P (2002) Developmental plasticity and growth rates of green frog (Rana clamitans) embryos and tadpoles in relation to a leech (Macrobdella decora) predator. Copeia 2002:445–449CrossRefGoogle Scholar
  53. Schotthoefer AM, Koehler AV, Meteyer CU, Cole RA (2003) Influence of Ribeiroia ondatrae (Trematoda: Digenea) infection on limb development and survival of northern leopard frogs (Rana pipiens): effects of host stage and parasite-exposure level. Can J Zool 81:1144–1153CrossRefGoogle Scholar
  54. Sih A, Moore RD (1993) Delayed hatching of salamander eggs in response to enhanced larval predation risk. Am Nat 142:947–960PubMedCrossRefGoogle Scholar
  55. Smith GR, Fortune DT (2009) Hatching plasticity of wood frog (Rana sylvatica) eggs in response to mosquitofish (Gambusia affinis) cues. Herpetol Conserv Biol 4:43–47Google Scholar
  56. Sollid SA, Lorz HV, Stevens DG, Bartholomew JL (2003) Age-dependent susceptibility of Chinook salmon to Myxobolus cerebralis and effects of sustained parasite challenges. J Aquat Anim Health 15:136–146CrossRefGoogle Scholar
  57. Stelkens RB, Jaffuel G, Escher M, Wedekind C (2012) Genetic and phenotypic population divergence on a microgeographic scale in brown trout. Mol Ecol 21:2896–2915PubMedCrossRefGoogle Scholar
  58. Touchon J, Gomez-Mestre I, Warkentin K (2006) Hatching plasticity in two temperate anurans: responses to a pathogen and predation cues. Can J Zool 84:556–563CrossRefGoogle Scholar
  59. Via S (1984) The quantitative genetics of polyphagy in an insect herbivore. II. Genetic correlations in larval performance within and among host plants. Evolution 38:896–905CrossRefGoogle Scholar
  60. von Siebenthal BA, Jacob A, Wedekind C (2009) Tolerance of whitefish embryos to Pseudomonas fluorescens linked to genetic and maternal effects, and reduced by previous exposure. Fish Shellfish Immunol 26:531–535CrossRefGoogle Scholar
  61. Vonesh JR (2005) Egg predation and predator-induced hatching plasticity in the African reed frog, Hyperolius spinigularis. Oikos 110:241–252CrossRefGoogle Scholar
  62. Warkentin KM (2007) Oxygen, gills, and embryo behavior: mechanisms of adaptive plasticity in hatching. Comp Biochem Physiol A 148:720–731CrossRefGoogle Scholar
  63. Warkentin KM (2011) Environmentally cued hatching across taxa: embryos respond to risk and opportunity. Integr Comp Biol 51:14–25PubMedCrossRefGoogle Scholar
  64. Warkentin KM, Currie CR, Rehner SA (2001) Egg-killing fungus induces early hatching of red-eyed treefrog eggs. Ecology 82:2860–2869CrossRefGoogle Scholar
  65. Wedekind C (2002) Induced hatching to avoid infectious egg disease in whitefish. Curr Biol 12:69–71PubMedCrossRefGoogle Scholar
  66. Wedekind C, Müller R (2005) Risk-induced early hatching in salmonids. Ecology 86:2525–2529CrossRefGoogle Scholar
  67. Wedekind C, Walker M, Portmann J, Cenni B, Müller R, Binz T (2004) MHC-linked susceptibility to a bacterial infection, but no MHC- linked cryptic female choice in whitefish. J Evol Biol 17:11–18PubMedCrossRefGoogle Scholar
  68. Wedekind C, Jacob A, Evanno G, Nusslé S, Müller R (2008) Viability of brown trout embryos positively linked to melanin-based but negatively to carotenoid-based colours of their fathers. Proc R Soc Lond B 275:1737–1744CrossRefGoogle Scholar
  69. Werner EE (1986) Amphibian metamorphosis: growth-rate, predation risk, and the optimal size at transformation. Am Nat 128:319–341CrossRefGoogle Scholar
  70. Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size structured populations. Annu Rev Ecol Syst 15:393–425CrossRefGoogle Scholar
  71. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Manuel Pompini
    • 1
  • Emily S. Clark
    • 1
  • Claus Wedekind
    • 1
  1. 1.Department of Ecology and Evolution, BiophoreUniversity of LausanneLausanneSwitzerland

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