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Oecologia

, Volume 160, Issue 1, pp 9–14 | Cite as

Pre-hatching exposure to water mold reduces size at metamorphosis in the moor frog

  • Tobias Uller
  • Jörgen Sagvik
  • Mats Olsson
Physiological Ecology - Original Paper

Abstract

Developmental plasticity is increasingly recognized as important for ecological and evolutionary processes. However, few studies consider the potential for delayed effects of early environments. Here, we show that tadpoles hatching from clutches exposed to water mold (Saprolegnia) have 20% decreased mass at metamorphosis, despite no further exposure subsequent to hatching. The effects were consistent across four populations that have previously been shown to vary in their resistance to infection during embryonic development. Contrary to expectations, time to hatching or metamorphosis was not affected, suggesting that the results do not reflect an evolved escape strategy from infected waters triggered by embryonic conditions. Instead, decreased mass at metamorphosis may arise from carry-over effects of impaired embryo development. Such strong links across developmental stages have potential consequences for the evolution of plasticity and the responses of populations to emergent infections.

Keywords

Amphibia Carry-over effects Developmental plasticity Metamorphosis Saprolegnia 

Notes

Acknowledgments

F. Simonson and T. Stenlund assisted in the field and laboratory. Two anonymous reviewers provided valuable suggestions that improved the paper. This work was supported by the Wenner–Gren Foundations (T. U.) and Formas (M. O. and J. S.). All experimental procedures comply with Swedish law and animal ethics regulations.

References

  1. Altwegg R, Reyer HU (2003) Patterns of natural selection on size at metamorphosis in water frogs. Evolution 57:872–882PubMedGoogle Scholar
  2. Bateson P, Barker D, Clutton-Brock T, Deb D, D’Udine B, Foley RA, Gluckman P, Godfrey K, Kirkwood T, Lahr MM, McNamara J, Metcalfe NB, Monaghan P, Spencer HG, Sultan SE (2004) Developmental plasticity and human health. Nature 430:419–421PubMedCrossRefGoogle Scholar
  3. Benard MF, Fodyce JA (2003) Are induced defenses costly? Consequences of predator-induced defenses in western toads, Bufo boreas. Ecology 84:68–78CrossRefGoogle Scholar
  4. Benard MF, McCauley SJ (2008) Integrating across life-history stages: consequences of natal habitat effects on dispersal. Am Nat 171:553–567PubMedCrossRefGoogle Scholar
  5. Blaustein AR, Hokit DG, Ohara RK, Holt RA (1994) Pathogenic fungus contributes to amphibian losses in the Pacific-Northwest. Biol Conserv 67:251–254CrossRefGoogle Scholar
  6. Capellan E, Nicieza AG (2007) Trade-offs across life stages: does predator-induced hatching plasticity reduce anuran post-metamorphic performance? Evol Ecol 21:445–458CrossRefGoogle Scholar
  7. De Block M, Stoks R (2005) Fitness effects from egg to reproduction: bridging the life history transition. Ecology 86:185–197CrossRefGoogle Scholar
  8. Densmore CL, Green DE (2007) Diseases of amphibians. ILAR J 48:235–254PubMedGoogle Scholar
  9. Fernandez-Beneitez MJ, Ortiz-Santaliestra ME, Lizana M, Dieguez-Uribeondo J (2008) Saprolegnia diclina: another species responsible for the emergent disease ‘Saprolegnia infections’ in amphibians. FEMS Microbiol Lett 279:23–29PubMedCrossRefGoogle Scholar
  10. Glandt D (2008) The moor frog, Rana arvalis: morphology, behavior, ecology & conservation. Laurenti, GermanyGoogle Scholar
  11. Gluckman PD, Hanson MA, Spencer HG (2005) Predictive adaptive responses and human evolution. Trends Ecol Evol 20:527–533PubMedCrossRefGoogle Scholar
  12. 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
  13. Gomez-Mestre I, Wiens JJ, Warkentin KM (2008) Evolution of adaptive plasticity: risk-sensitive hatching in Neotropical leaf-breeding treefrogs (Agalychnis: Hylidae). Ecol Monogr 78:205-224Google Scholar
  14. Gorman HE, Nager RG (2004) Prenatal developmental conditions have long-term effects on offspring fecundity. Proc R Soc Lond B 271:1923–1928CrossRefGoogle Scholar
  15. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190Google Scholar
  16. Groothuis TGG, Schwabl H (2008) Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Philos Trans R Soc Lond B 363:1647–1661CrossRefGoogle Scholar
  17. Hamdoun A, Epel D (2007) Embryo stability and vulnerability in an always changing world. Proc Natl Acad Sci USA 104:1745–1750PubMedCrossRefGoogle Scholar
  18. Kiesecker JM, Blaustein AR (1999) Pathogen reverses competition between larval amphibians. Ecology 80:2442–2448Google Scholar
  19. Laurila A, Pakkasmaa S, Crochet P-A, Merilä J (2003) Predator-induced plasticity in early life history and morphology in two anuran amphibians. Oecologia 132:524–530CrossRefGoogle Scholar
  20. Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348PubMedCrossRefGoogle Scholar
  21. Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS system for mixed models, 2nd edn. SAS Institute, CaryGoogle Scholar
  22. Marshall DJ (2008) Transgenerational plasticity in the sea: context-dependent maternal effects across life history stages. Ecology 89:418–427PubMedCrossRefGoogle Scholar
  23. Monaghan P (2008) Early growth conditions, phenotypic development and environmental change. Philos Trans R Soc Lond B 363:1635–1645CrossRefGoogle Scholar
  24. Nicieza AG, Alvarez D, Atienza EMS (2006) Delayed effects of larval predation risk and food quality on anuran juvenile performance. J Evol Biol 19:1092–1103PubMedCrossRefGoogle Scholar
  25. Pahkala M, Laurila A, Merilä J (2001) Carry-over effects of ultraviolet-B radiation on larval fitness in Rana temporaria. Proc R Soc Lond B 268:1699–1706CrossRefGoogle Scholar
  26. Pechenik JA (2006) Larval experience and latent effects—metamorphosis is not a new beginning. Integr Comp Biol 46:323–333CrossRefGoogle Scholar
  27. Räsänen K, Laurila A, Merilä J (2002) Carry-over effects of embryonic acid conditions on development and growth of Rana temporaria tadpoles. Freshwater Biol 47:19–30CrossRefGoogle Scholar
  28. Relyea RA (2001) The lasting effects of adaptive plasticity: predator-induced tadpoles become long-legged frogs. Ecology 82:1947–1955CrossRefGoogle Scholar
  29. Rickard IJ, Lumma V (2007) The predictive adaptive response and metabolic syndrome—challenges for the hypothesis. Trends Endocrinol Metab 18:94–99PubMedCrossRefGoogle Scholar
  30. Sagvik J, Uller T, Stenlund T, Olsson M (2008a) Intraspecific variation in resistance of frog eggs to fungal infection. Evol Ecol 22:193–201CrossRefGoogle Scholar
  31. Sagvik J, Uller T, Olsson M (2008b) A genetic component of resistance to fungal infection in frog embryos. Proc R Soc Lond B 275:1393–1396CrossRefGoogle Scholar
  32. Sakata JT, Crews D (2004) Developmental sculpting of social phenotype and plasticity. Neurosci Biobehav Rev 28:95–112PubMedCrossRefGoogle Scholar
  33. Schlichting CD, Pigliucci M (1998) phenotypic evolution: a reaction norm perspective. Sinauer, SunderlandGoogle Scholar
  34. Touchon JC, Gomez-Mestre I, Warkentin KM (2006) Hatching plasticity in two temperate anurans: responses to a pathogen and predation cues. Can J Zool 84:556–563CrossRefGoogle Scholar
  35. Uller T (2008) Developmental plasticity and the evolution of parental effects. Trends Ecol Evol 23:432–438PubMedCrossRefGoogle Scholar
  36. Uller T, Massot M, Richard M, Lecomte J, Clobert J (2004) Long-lasting fitness consequences of prenatal sex ratio in a viviparous lizard. Evolution 58:2511–2516PubMedGoogle Scholar
  37. Uller T, Isaksson C, Olsson M (2006a) Immune challenge reduces reproductive output and growth in a lizard. Funct Ecol 20:873–879CrossRefGoogle Scholar
  38. Uller T, Andersson S, Eklöf J (2006b) Juvenile cell mediated immune response is negatively correlated with subsequent adult ornament size in quail. Evol Ecol 20:1–9CrossRefGoogle Scholar
  39. Van Buskirk J, Saxer G (2001) Delayed costs of an induced defense in tadpoles? Morphology, hopping and developmental rate at metamorphosis. Evolution 55:821–829PubMedCrossRefGoogle Scholar
  40. van Gelder JJ, Wijnands HEJ (1987) Twenty years of ecological investigation on the moor frog (Rana arvalis). Beih Schriftenr Naturschutz Landschaftspfl Niedersachs 19:141–145Google Scholar
  41. Vonesh JR, Bolker BM (2005) Compensatory larval responses shift trade-offs associated with predator-induced hatching plasticity. Ecology 86:1580–1591CrossRefGoogle Scholar
  42. Warkentin KM (2007) Oxygen, gills, and embryo behavior: mechanisms of adaptive plasticity in hatching. Comp Biochem Physiol A 148:720–731CrossRefGoogle Scholar
  43. Welberg LAM, Seckl JR (2001) Prenatal stress, glucocorticoids and the programming of the brain. J Neuroendocrinol 13:113–128PubMedCrossRefGoogle Scholar
  44. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New YorkGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Department of Zoology, Edward Grey InstituteUniversity of OxfordOxfordUK
  2. 2.Institute for Conservation BiologyUniversity of WollongongWollongongAustralia
  3. 3.Department of ZoologyUniversity of GothenburgGöteborgSweden

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