Department Aquatic Ecology

Adaptive divergence in response to environmental stress – amphibians along an acidification gradient

Why this project?  Environmental stress is a major ecological and evolutionary force, driving shifts in species distribution and intra-specific phenotypic divergence. We currently study the role of physiology in adaptive divergence to environmental stress and the genomic basis of physiology and maternal effect mediated adaptation.

Acid stress: Human induced acidification has resulted in severe reductions in pH since the industrial revolution, in both aquatic and terrestrial systems.  Acid stress has strong negative consequences on organismal fitness and thereby causes strong natural selection. Acid stress reduces individual growth rates, survival and reproduction. Furthermore, acidification causes large shifts in ecological communities (e.g. predators, parasites and fungal pathogens) and abiotic factors (e.g. increased metal leeching). These correlated changes can result in multifarious selection in response to acidification. Natural populations inhabiting environments that differ in pH due to natural and/or human induced acidification provide a good model system for testing how organisms adapt to both pH and interacting environmental stressors.

Evolutionary physiology (NEW SNF PROJECT): In vertebrates, corticosterone (CORT) is a key stress hormone. CORT levels are often elevated in short term stress responses - to facilitate adaptive physiological responses - but can come at a cost under long-term stress.
Moreover, the CORT hormonal pathway influences the expression of gene networks related to metabolism, growth, repair, reproduction, the management of resource allocation and immune function. Hence, populations differing in the magnitude or type of environmental stress should be under divergent selection on physiological stress responses.
Of key importance in relation to acidification mediated natural selection in amphibians, is that CORT affects behavioral activity and predator defense traits (e.g. tail depth), that CORT levels are elevated in response to acidic pH and predator presence and that trematode parasites (that use tadpoles as hosts) are lost in acidic environments. As pH, predation and parasites change simultaneously due to acidification we test the predictions that I) acidification causes divergent selection via acid stress tolerance, predator defense and immune defense traits and II) the responses to these correlated selective agents can be mediated through the CORT pathway (providing a “magic” link to multifarious divergent selection).

Egg coats: Maternal effects are often key adaptations during early life-stages, and can allow rapid adaptation or alter direction of evolution. One important, but relatively little studied, source of maternal effects in various taxa are egg coats (maternally derived extracellular matrix that surrounds the embryos). These can have strong effects on reproductive success in natural populations, as they can influence sperm-egg interactions as well embryonic performance under different abiotic and biotic conditions. In amphibians, the egg coats are multilayered structures consisting primarily of glycoproteins. In acidic conditions, egg coats undergo chemical changes and can become a trap for the developing embryo (i.e. so called “curling defect” that results in hatching failure).

Study system: In this core project, we study adaptive divergence of amphibian populations (focusing on the moor frog, Rana arvalis) along an acidification gradient in SW Sweden. In this area, amphibian breeding pond pH can range from 4 to 7. 

Approaches: We apply a combination of empirical approaches, ranging from laboratory common garden experiments, quantitative genetics and standard population genetics approaches to – omics tools (genomics, proteomics, transcriptomics, glycomics).

What have we found so far?

  • R. arvalis (RA) shows adaptive divergence in embryonic acid stress tolerance, larval life-history traits, anti-predator defenses and maternal investment along the acidification gradient.
  • The degree of phenotypic divergence in RA is related to the magnitude of differences in breeding pond pH, indicating that pH reflects variation in the strength of divergent selection. Moreover, RA appears to be responding to multiple selective agents simultaneously (e.g. pH and predators).
  • The mechanisms underlying divergence in RA include both maternal (esp. egg coats and egg size) and direct genetic effects.
  • Egg jelly coats harbour extensive within species molecular variation, whereby jelly coat glycoproteins influence water balance at acidic pH (providing a mechanism for the curling defect).

Ongoing and upcoming: Ongoing work focuses on the molecular and physiological underpinnings of adaptive divergence in relation to pH and correlated selective agents. We now use transcriptomics and SNP genotyping to investigate the molecular genetic basis of adaptive divergence in R. arvalis. In addition to physiological processes, a new dimension is to investigate the role of trematode parasites as agent of natural selection in tadpoles.

Key collaborators: Prof. Anssi Laurila (Uppsala University, Sweden), Dr. Otto Seppälä (Eawag/ETH-Z, Switzerland), Dr. Marc Suter (Eawag, Switzerland), Dr. Longfei Shu (Washington Univ., St Louis, USA).

Related publications (own student papers):

Conceptual reviews:

Shu, L, Suter, M-F & Räsänen, K*. (2015). Evolution of egg coats: linking molecular biologyand ecology. Mol. Ecol., 24, 4052-73 (Invited reviews and syntheses).

Räsänen, K & Hendry, AP. (2008) Disentangling interactions between adaptive divergence
and gene flow when ecology drives diversification. Ecol. Lett. 11, 624-636.

Räsänen, K & Kruuk, LEB. (2007) Maternal effects and evolution at ecological time scales. Func. Ecol. 21, 408-421.

Empirical:

Shu L, Laurila A, Suter M, Räsänen K. (2016). Molecular phenotyping of maternally mediated parallel adaptive divergence within Rana arvalis and Rana temporaria. Mol. Ecol., 25, 4564 -4579

Shu L, Suter M-F, Laurila, A & Räsänen, K. (2015) Environmental stress mediated adaptive divergence in ion channel function during embryogenesis in Rana arvalis, Sci. Rep. Sci. Rep. doi: 10.1038/srep14201.

Shu, L, Suter M-F, Laurila, A & Räsänen, K. (2015). Mechanistic basis of adaptive maternal effects: egg jelly water balance mediates embryonic adaptation to acidity in Rana arvalis. Oecologia 179, 617-28.

Egea-Serrano, A, Hangartner, S, Laurila, A & Räsänen, K. (2014) Multifarious selection through environmental stress: pH and predation driven adaptive divergence of the moor frog (Rana arvalis). Proc. R. Soc. B. 281, 20133266.

Hangartner, S, Laurila, A & Räsänen K. (2012) The quantitative genetic basis of adaptive
divergence in the moor frog (Rana arvalis) and its implications for gene flow. J. Evol. Biol. 66, 867-881.

People

Dr. Katja RäsänenTel. +41 58 765 5186Send Mail
Dr. Marc SuterDeputy Department HeadTel. +41 58 765 5479Send Mail

Publications

Conceptual

Shu, L.; Suter, M. J. -F.; Räsänen, K. (2015) Evolution of egg coats: linking molecular biology and ecology, Molecular Ecology, 24(16), 4052-4073, doi:10.1111/mec.13283, Institutional Repository
Räsänen, K.; Hendry, A. P. (2008) Disentangling interactions between adaptive divergence and gene flow when ecology drives diversification, Ecology Letters, 11(6), 624-636, doi:10.1111/j.1461-0248.2008.01176.x, Institutional Repository
Räsänen, K.; Kruuk, L. E. B. (2007) Maternal effects and evolution at ecological time-scales, Functional Ecology, 21(3), 408-421, doi:10.1111/j.1365-2435.2007.01246.x, Institutional Repository

Empirical

Shu, L.; Suter, M. J. -F.; Laurila, A.; Räsänen, K. (2015) Mechanistic basis of adaptive maternal effects: egg jelly water balance mediates embryonic adaptation to acidity in Rana arvalis, Oecologia, 179(3), 617-628, doi:10.1007/s00442-015-3332-4, Institutional Repository
Egea-Serrano, A.; Hangartner, S.; Laurila, A.; Räsänen, K. (2014) Multifarious selection through environmental change: acidity and predator-mediated adaptive divergence in the moor frog (Rana arvalis), Proceedings of the Royal Society B: Biological Sciences, 281(1780), 20133266 (10 pp.), doi:10.1098/rspb.2013.3266, Institutional Repository
Hangartner, S.; Laurila, A.; Räsänen, K. (2012) The quantitative genetic basis of adaptive divergence in the moor frog (Rana arvalis) and its implications for gene flow, Journal of Evolutionary Biology, 25(8), 1587-1599, doi:10.1111/j.1420-9101.2012.02546.x, Institutional Repository
Hangartner, S.; Laurila, A.; Räsänen, K. (2012) Adaptive divergence in moor frog (rana arvalis) populations along an acidification gradient: inferences from QST-FST correlations, Evolution, International Journal of Organic Evolution, 66(3), 867-881, doi:10.1111/j.1558-5646.2011.01472.x, Institutional Repository
Rasanen, K.; Söderman, F.; Laurila, A.; Merilä, J. (2008) Geographic variation in maternal investment: acidity affects egg size and fecundity in Rana arvalis, Ecology, 89(9), 2553-2562, doi:10.1890/07-0168.1, Institutional Repository
Persson, M.; Räsänen, K.; Laurila, A.; Merilä, J. (2007) Maternally determined adaptation to acidity in Rana arvalis: are laboratory and field estimates of embryonic stress tolerance congruent?, Canadian Journal of Zoology, 85(7), 832-838, doi:10.1139/Z07-064, Institutional Repository
Teplitsky, C.; Räsänen, K.; Laurila, A. (2007) Adaptive plasticity in stressful environments: acidity constrains inducible defences in Rana arvalis, Evolutionary Ecology Research, 9(3), 447-458, Institutional Repository
Räsänen, K.; Laurila, A.; Merilä, J. (2005) Maternal investment in egg size: environment- and population-specific effects on offspring performance, Oecologia, 142(4), 546-553, doi:10.1007/s00442-004-1762-5, Institutional Repository
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, Conservation Genetics, 5(4), 513-527, doi:10.1023/B:COGE.0000041026.71104.0a, Institutional Repository
Räsänen, K.; Laurila, A.; Merilä, J. (2003) Geographic variation in acid stress tolerance of the moor frog, Rana arvalis. I. Local adaptation, Evolution, International Journal of Organic Evolution, 57(2), 352-362, doi:10.1111/j.0014-3820.2003.tb00269.x, Institutional Repository
Räsänen, K.; Laurila, A.; Merilä, J. (2002) Carry-over effects of embryonic acid conditions on development and growth of Rana temporaria tadpoles, Freshwater Biology, 47(1), 19-30, doi:10.1046/j.1365-2427.2002.00777.x, Institutional Repository
Pahkala, M.; Räsänen, K.; Laurila, A.; Johanson, U.; Björn, L. O.; Merilä, J. (2002) Lethal and sublethal effects of UV-B/pH synergism on common frog embryos, Conservation Biology, 16(4), 1063-1073, doi:10.1046/j.1523-1739.2002.00527.x, Institutional Repository

Book chapters

Räsänen,K.; Green,D.M.; (2009) Acidification and its effects on amphibian populations. In Amphibian Biology, Volume 8. Decline: Diseases, Parasites, Maladies and Pollution. H. Heatwole (ed.), Surrey Beatty and Sons, Chipping Norton, Australia; 3244-3267.

Related student projects

Ph.D. theses

Shu Longfei (2014) The Molecular Basis of Embryonic Adaptation to Acid Stress in Amphibians. Diss. ETH Nr. 22319. Dept. of Aquatic Ecology, Eawag/Institute of Integrative Biology, ETH -Zurich, Switzerland.

Hangartner Sandra (2010) Adaptive divergence of the moor frog (Rana arvalis) along an acidification gradient. Diss ETH nr: 19384. Dept. of Aquatic Ecology, Eawag/Institute of Integrative Biology, ETH-Zurich, Switzerland.

M.Sc. theses

Schenkel Corinne (2013) The role of egg capsules in resistance to Saprolegnia in Rana arvalis and R. temporaria. Univ. of Zurich, Switzerland.

Krähenbühl Kim (2011) Among population divergence in embryonic response of Rana arvalis to interactions of pH and Saprolegnia infections. Dept. of Biology, ETH-Zurich, Switzerland.

Riedener Eliane (2010) Adaptive divergence in embryonic acid stress tolerance of Rana arvalis: the role of microhabitat variation in a reciprocal transplant experiment”. Dept.of Environmental sciences, ETH-Zurich, Switzerland.

Brunold Claudio (2009). Acid stress tolerance and adaptive maternal effects of Rana arvalis and Rana temporaria. Dept. of Biology, ETH-Zurich, Switzerland.

Persson Mikael (2003) Local adaptation to acid stress in the moor frog - a field experiment. Uppsala University, Sweden.