Abstract
As potential to adapt to environmental stress can be essential for population persistence, knowledge on the genetic architecture of local adaptation is important for conservation genetics. We investigated the relative importance of additive genetic, dominance and maternal effects contributions to acid stress tolerance in two moor frog (Rana arvalis) populations originating from low and neutral pH habitats. Experiments with crosses obtained from artificial matings revealed that embryos from the acid origin population were more tolerant to low pH than embryos from the neutral origin population in embryonic survival rates, but not in terms of developmental stability, developmental and growth rates. Strong maternal effect and small additive genetic contributions to variation were detected in all traits in both populations. In general, dominance contributions to variance in different traits were of similar magnitude to the additive genetic effects, but dominance effects outweighed the additive genetic and maternal effects contributions to early growth in both populations. Furthermore, the expression of additive genetic variance was independent of pH treatment, suggesting little additive genetic variation in acid stress tolerance. The results suggest that although local genetic adaptation to acid stress has taken place, the current variation in acid stress tolerance in acidified populations may owe largely to non-genetic effects. However, low but significant heritabilities (h 2≈ 0.07–0.22) in all traits – including viability itself – under a wide range of pH conditions suggests that environmental stress created by low pH is unlikely to lower moor frog populations' ability to respond to selection in the traits studied. Nevertheless, acid conditions could lower populations' ability to respond to selection in the long run through reduction in effective population size.
Similar content being viewed by others
References
Alford RA, Richards S (1999) Global amphibian declines: A problem in applied ecology. Annu. Rev. Ecol. Syst., 30, 109–132.
Andrén C, Herikson L, Olson M, Nilsson G (1988) Effects of pH and aluminium on embryonic and early larval stages of Swedish brown frogs Rana arvalis, R. temporaria and R. dalmatina. Holarctic Ecol., 11, 127–135.
Andrén C, Mårdén M, Nilsson G (1989) Tolerance to low pH in a population of moor frogs, Rana arvalis, from an acid and a neutral environment: A possible case of rapid evolutionary response to acidi cation. Oikos, 56, 215–223.
APHA (1985) Standard Methods for the Examination of Water and Wastewater, 16th edn. American Public Health Association, Washington, DC.
Becker WA (1985) Manual of Quantitative Genetics, 4th edn. Academic Enterprises, Pullman.
Beebee TJC (1995) Amphibian breeding and climate. Nature, 374, 219–220.
Beebee TJC (1996) Ecology and Conservation of Amphibians. Chapman & Hall, London.
Bertils U, Hanneberg P (1995) Försurningen i Sverige–vad vet vi egentligen? Rapport 4421, Naturvårdsverket, Stockholm.
Berven KA, Gill DE (1983) Interpreting geographical variation in life-history traits. Am. Zool., 23, 85–97.
Billington HL, Pelham J (1991) Genetic variation in the date of budburst in Scottish birch populations–implications for climate change. Funct. Ecol., 5, 403–409.
Blows MW, Sokolowski MB (1995) The expression of additive and nonadditive genetic variation under stress. Genetics, 140, 1149–1159.
Böhmer J, Rahmann H (1990) Influence of surface water acidi cation on amphibians. In: Biology and Physiology of Amphibians (ed. Hanke W), pp. 287–309. Gustav Fisher Verlag, Stuttgart.
Brakke DF, Baker JP, Böhmer J, Hartmann A, Havas M, Jenkins A, Kelly C, Ormerod SJ, Paces T, Putz R, Rosseland BO, Schindler DW, Segner H (1994) Group report: physiological and ecological effects of acidi cation on aquatic biota. In: Acidication of Freshwater Ecosystems: Implications for the Future (eds. Steinberg CEW, Wright RF), pp. 275–312. John Wiley & Sons Ltd, Chichester.
Breslow NE, Clayton DG (1993) Approximate inference in generalized linear mixed models. J. Am. Stat. Assoc., 88, 9–25.
Bürger RL, Lynch M (1997) Adaptation and extinction in changing environments. In: Environmental Stress, Adaptation and Evolution (eds. Bijlsma R, Loeschkcke V), pp. 209–240. Springer Verlag, Berlin.
Clark KL, LaZerte BD (1987) Intraspeci c variation in hydrogen ion and aluminum toxicity in Bufo americanus and Ambystoma maculatum. Can. J. Fish. Aquat. Sci., 44, 1622–1628.
Clausnitzer HJ (1987) Gefä hrdung des moorfrosches (Rana arvalis) durch versauerung der laichgewässer. Naturschutz und Landschaftspl. Niedersachsen, Hannover, Beiheft, 19, 131–138.
Collins JP, Storfer A (2003) Global amphibian declines: Sorting the hypothesis. Divers. Distribut., 9, 89–98.
Crnokrak P, Ro. DA (1995) Dominance variance: Associations with selection and tness. Heredity, 75, 530–540.
Edwards DJ, Hjeldnes S (1977) Growth and Survival of Salmonids in Waters of Different pH. SNSP project, Norway, Fr, 10/77, 12 pp.
Einum S, Fleming IA (1999) Maternal effects of egg size in brown trout (Salmo trutta): Norms of reaction to environmental quality. Proc. R. Soc. Lond. B, 266, 2095–2100.
Elmberg J (1984) Åkergrodan Rana arvalis Nilsson i norra Sverige. Fauna och Flora, 79, 69–77.
Fog K, Schmedens A, Rosenørnde Lasson D (1997) Nordens padder og krybdyr. G. E. C. Gads Forlag, Copenhagen.
Forbes VE (1999) Genetics and Ecotoxicology. Taylor & Francis, London.
Forbes VE, Calow P (1997) Responses of aquatic organisms to pollutant stress: theoretical and practical implications. In: Environmental Stress, Adaptation and Evolution (eds. Bijlsma R, Loeschkcke V), pp. 25–42. Springer Verlag, Berlin.
Freda J (1986) The influence of acidic pond water on amphibians–a review. Water Air Soil Pollut., 30, 439–450.
Gasc JP, Cabela A, Crnobrnja-Isailovic J, Dolmen D, Grossenbacher K, Haffner P, Lescure J, Martens H, Martinez JP, Maurin H, Oliveira ME, Sofiandiou TS, Veith M, Zuiderwijk A (eds.) (1997). Atlas of Amphibians and Reptiles in Europe. Societeas Europaea Herpetologica & Muséum National d'Historie Naturelle (IEGB/SPN), Paris.
Gelman A, Carlin JB, Stern H, Rubin DB (1995) Bayesian Data Analysis. Chapman & Hall, London.
Gislén T, Kauri H (1959) Zoogeography of the Swedish amphibians and reptiles with notes on their growth and ecology. Acta Vert., 1, 193–397.
Gjedrem T (1976) Genetic Variation in Tolerance of Brown Trout to Acid Water. SNSF project, Norway FR 5/76, 1–11.
Gosner KL (1960) A simpli ed table for staging anuran embryos and larvae with notes on identi cation. Herpetologica, 16, 183–190.
Gosner KL, Black IH (1957) The effects of acidity on the development and hatching of new Jersey frogs. Ecology, 38, 256–262.
Hesthagen T, Sevaldrud IH, Berger HM (1999) Assessment of damage to sh populations in norwegian lakes due to acidification. Ambio, 28, 112–117.
Hoffmann AA, Hercus MJ (2000) Environmental stress as an evolutionary force. BioScience, 50, 217–226.
Hoffmann AA, Merilä J (1999) Heritable genetic variation and evolution under favourable and unfavourable conditions. Trends Ecol. Evol., 14, 96–101.
Houlahan JE, Findlay CS, Schmidt BR (2000) Quantitative evidence for global amphibian population declines. Nature, 404, 752–755.
Houle D (1992) Comparing evolvability and variability of quantitative traits. Genetics, 130, 195–204.
Hulme M, Barrow EM, Arnell NW, Harrison PA, Johns TC, Dowing TE (1999) Relative impacts of human-induced climate change and natural climate variability. Nature, 397, 688–691.
Ishchenko V (1997) Rana arvalis Nilsson, 1842. In: Atlas of Amphibians and Reptiles in Europe (eds. Gasc JP, Cabela A, Crnobrnja-Isailovic J, Dolmen D, Grossenbacher K, Haffner P, Lescure J, Martens H, Martinez JP, Maurin H, Oliveira ME, Sofiandiou TS, Veith M, Zuiderwijk A), pp. 128–129. Societeas Europaea Herpetologica & Muséum National d 'Historie Naturelle (IEGB/SPN), Paris.
Kaplan RH (1992) Greater maternal investment can decrease o. spring survival in the frog Bombina orientalis. Ecology, 73, 280–288.
Kaplan RH (1998) Maternal effects, developmental plasticity and life history evolution. An amphibian model. In: Maternal Effects as Adaptations (eds. Mousseau TH, Fox CW), pp. 244–260. Oxford University Press, New York.
Kareiva PM, Kingsolver JG, Huey R (1993) Biotic Interactions and Global Change. Sinauer Associates Inc., Sunderland, MA.
Karns RH (1992) Effects of acidic bog habitats on amphibian reproduction in a northern Minnesota peatland. J. Herpetol., 26, 401–412.
Kearsey MJ, Pooni HS (1996) The Genetical Analysis of Quantitative Traits. Chapman & Hall, London.
Kruuk LEB, Clutton-Brock TH, Slate J, Pemberton JM, Brotherstone S, Guiness FE (2000) Heritability of tness in a wild mammal population. Proc. Natl. Acad. Sci. USA, 97, 698–703.
Lardner B (1998) Plasticity or xed adaptive traits?Strategies for predation avoidance in Rana arvalis tadpoles. Oecologia, 117, 119–126.
Laugen AT, Laurila A, Merilä J (2002) Maternal and genetic contributions to geographical variation in Rana temporaria larval life-history traits. Biol. J. Linn. Soc., 76, 61–70.
Laugen AT, Laurila A, Räsänen K, Merilä J (2003) Latitudinal countergradient variation in the common frog (Rana temporaria) development rates–evidence for local adaptation. J. Evol. Biol., 16, 996–1005.
Leuven RSEW, den Hartog C, Christiaans MMC, Heijligers WHC (1986) Effects of water acidi cation on the distribution pattern and the reproductive success of amphibians. Experientia, 42, 495–503.
Licht LE (1996) Amphibian decline still a puzzle. BioScience, 46, 172–173.
Lynch M, Lande R (1993) Evolution and extinction in response to environmental change. In: Biotic Interactions and Global Change (eds. Kareiva PM, Kingsolver JG, Huey RB), pp. 234–250. Sinauer Associates Inc., Sunderland, Massachusetts.
Lynch M, Walsh B (1998) Genetics and Analysis of Quantitative Traits. Sinauer Associates Inc., Publishers, Sunderland, MA.
Madronich S, McKenzie RL, Björn LO, Caldwell MM (1998) Changes in biologically active ultraviolet radiation reaching the Earth 's surface. J. Photochem. Biol., 46, 5–19.
McCullagh P, Nelder JA (1989) Generalized Linear Models, 2nd edn. Chapman & Hall, London.
Menzel A, Fabian P (1999) Growing season extended in Europe. Nature, 397, p. 659.
Merilä J, Sheldon BC (1999) Genetic architecture of tness and non-tness traits–empirical patterns and development of ideas. Heredity, 83, 103–109.
Merilä J, Sheldon BC (2000) Lifetime reproductive success and heritability in nature. Am. Nat., 155, 301–310.
Mousseau TH, Fox CW (1998) Maternal Effects as Adaptations. Oxford University Press, New York.
Muniz I, Grande M (1974) A report in SNSP project, Norway, FR 3/74, 29–39.
NIH (1998) NIH Image, ver. 1. 61. National Institutes of Health, USA.
Pakkasmaa S, Merilä J, O'Hara R (2003) Genetic and maternal effect influences on viability of common frog tadpoles under di. erent environmental conditions. Heredity, 91, 117–124.
Parichy DM, Kaplan RH (1992) Maternal effects on offspring growth and development depend on environmental quality in the frog Bombina orientalis. Oecologia, 91, 579–586.
Parmesan C, Yohe G (2003) A globally coherent ngerprint of climate change impacts across natural systems. Nature, 421, 37–42.
Pechmann JHK, Scott DE, Semlitch RD, Caldwell JP, Vitt LJ, Gibbons JW (1991) Declining amphibian populations: the problem of separating human impacts from natural fluctuations. Science, 253, 892–895.
Picker MD, McKenzie CJ, Fielding P (1993) Embryonic tolerance of Xenopus (Anura) to acidic black water. Copeia, 1993, 1072–1081.
Pierce BA (1985) Acid tolerance in amphibians. BioScience, 35, 239–243.
Pierce BA, Harvey JM (1987) Geographic variation in acid stress tolerance of Connecticut wood frogs. Copeia, 1987, 94–103.
Pierce BA, Sikand N (1985) Intrapopulation variation in acid tolerance of Conneticut wood frogs: genetic and maternal effects. Can. J. Zool., 63, 1647–1651.
Pierce BA, Wooten DK (1992) Genetic variation in tolerance of amphibians to low pH. J. Herpetol., 26, 422–429.
Räsänen K (2002) Evolutionary Implications of acidification–A Frog 's Eye View. PhD thesis, Uppsala University.
Räsänen K, Laurila A, Merilä J (2003a) Geographic variation in acid stress tolerance of the moor frog, Rana arvalis. II. Adaptive maternal effects. Evolution, 57, 363–371.
Räsänen K, Laurila A, Merilä J (2003b) Geographic variation in acid stress tolerance of the moor frog, Rana arvalis. I. Local adaptation. Evolution, 57, 352–362.
Rosseland BO, Skogheim OK (1987) Differences in sensitivity to acidic soft-water among strains of brown trout (Salmo trutta L). Ann. Soc. R. Zool. Belg., 117, 255–264.
Rossiter M (1998) The role of environmental variation in parental effects expression. In: Maternal Effects as Adaptations (Eds. Fox M, Mousseau TA), pp. 113–134. Oxford University press, New York.
Semlitsch RD, Schmiedehausen S (1994) Parental contributions to variation in hatchling size and its relationship to growth and metamorphosis in tadpoles of Rana lessonae and Rana esculenta. Copeia, 1994, 406–412.
Speigelhalter DJ, Thomas A, Best NG (1999) WinBUGS Version 1.2 User Manual. MRC Biostatistics Unit, Cambridge, UK.
Spiegelhalter DJ, Best NG, Carlin BP, van der Linde A (2002) Bayesian measures of model complexity and fit (with discussion). J. R. Statist. Soc. B, 64, 583–640.
Swarts FA, Dunson WA, Wright JE (1978) Genetic and environmental factors involved in increased resistance of brook trout to sulphuric acid solutions and mine acid polluted waters. Trans. Amer. Fish. Soc., 107, 651–677.
Tyler-Jones R, Beattie RC, Aston RJ (1989) The effects of acid water and aluminium on the embryonic development of the common frog, Rana temporaria. J. Zool., 219, 355–372.
Wade MJ (1991) Genetic variance for rate of population increase in natural populations of flour beetles, Tribolium spp. Evolution, 45, 1574–1584.
Wake DB (1991) Declining amphibian populations. Science, 253, p. 860.
Wake DB (1998) Action on amphibians. Trends Ecol. Evol., 13, 379–380.
Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, et al. (2002) Ecological responses to recent climate change. Nature, 416, 389–395.
Ward RD, Skibinsky DOF, Woodwark M (1992) Protein heterozygosity, protein strucure and taxonomic differentiation. Evol. Biol., 26, 3–131.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Merilä, J., Söderman, F., O'Hara, R. et al. Local Adaptation and Genetics of Acid-Stress Tolerance in the Moor Frog, Rana arvalis . Conservation Genetics 5, 513–527 (2004). https://doi.org/10.1023/B:COGE.0000041026.71104.0a
Issue Date:
DOI: https://doi.org/10.1023/B:COGE.0000041026.71104.0a