In a remarkable example of recent frog adaptations we see how plasticity enables responses to unexpected environmental circumstances. The wood frog (Lithobates sylvaticus) is found throughout much of Canada, Alaska and the mid and eastern United States, living in wet woodlands that are swampy or have ponds. The extent of agriculture in North America results in woods being frequently close to farmed land, and these frogs consequently being exposed to pesticides. Research has shown that phenotypic plasticity provides them with a way to tolerate pesticide exposure, and is also generating permanent changes in this animal’s populations1.
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Carbaryl is a synthetic insecticide widely used in agriculture and horticulture. Woodland ponds may become exposed to Carbaryl as run-off from agricultural land, and it is toxic to aquatic animals including fish and amphibians. Clearly, ponds closer to agricultural land often have higher concentrations of Carbaryl pollution than those further away, so exposure of frogs to the insecticide is closely related to agricultural proximity. That in turn correlates with how sensitive the frogs are to its toxic effects. When tadpoles are exposed to Carbaryl in the laboratory, those from ponds close to agriculture are less susceptible to it (measured as the proportion of tadpoles that survive a known toxic dose) than those from ponds further away. (The distances from agriculture of ponds from which frog eggs were taken ranged from a few metres to about half a kilometre.) Being from sites with greater insecticide exposure therefore seems to have given tadpoles extra resistance to Carbaryl. These frog adaptations become even more interesting when we consider where that resistance comes from. Because it’s not that the tadpoles from agriculture-distant ponds don’t have Carbaryl resistance, only that it isn’t activated. If tadpoles are exposed to a low, non-lethal dose of Carbaryl for a period prior to being exposed to the toxic dose, the agriculture-distant ones become resistant to it. Pre-exposure of tadpoles from agriculture-proximate sites makes little difference to their degree of Carbaryl resistance. What this shows is that the ancestral condition of wood frogs (represented by those tadpoles from sites with little or no Carbaryl pollution) is that they have resistance that can be induced, whereas frogs from populations with experience of insecticide exposure have resistance that is permanently expressed (the term for which is constitutive).
Continued and biologically significant exposure to insecticide has caused a change in important biological processes within these frogs. The change to constitutive expression of resistance benefits them because they are in an environment where lethal pollution may be constant or frequent. Since they do not encounter resistance-inducing, low concentrations of pollutant, constant resistance to toxic concentrations is needed instead. These frogs have adapted to this severe environment and, importantly, that adaptation is innate, a genetic trait with which subsequent generations are born. Plasticity has therefore been the starting point for a change in the biology of these pollution-exposed frogs. A phenotypic variation in the form of a variable resistance has provided an advantage on which natural selection has been able to act, yielding a new, fixed and heritable phenotype which has better fitness in the altered, more adverse environment. (The experiment was carefully designed to discriminate between this mechanism and other ways in which the heritable resistance could potentially have occurred.)
” … a variable resistance has provided an advantage on which natural selection has been able to act, yielding a new, fixed and heritable phenotype which has better fitness in the altered, more adverse environment.”
That heritable fixation is termed assimilation2. It is not yet fully clear how assimilation takes place, but well established, related laboratory research has shown that it can be dependent on natural selection acting upon animals with altered plastic characteristics. It may be that processes activated by stress (in this case the toxic effect of the pollutant) are involved. There is evidence to suggest that animals carry genetic mutations whose effects are usually suppressed, but can be released by stress induced processes. These are called cryptic mutations, and certain of them might act to change inducible genes into constitutive ones3 4 5 6. Alternatively, a similar genetic change from inducible to constitutive phenotype might also be the result of stress increasing the rate of genetic mutation7.
This example of frog adaptations is one of plasticity in the animals’ biochemistry, but plasticity affects a range of biological phenomena including behaviour, ecological interactions and morphology. An example of the last is presented in the next section.
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References
- Hua, Jessica, Devin K. Jones, Brian M. Mattes, Rickey D. Cothran, Rick A. Relyea, and Jason T. Hoverman. ‘The Contribution of Phenotypic Plasticity to the Evolution of Insecticide Tolerance in Amphibian Populations’. Evolutionary Applications 8, no. 6 (July 2015): 586–96. https://doi.org/10.1111/eva.12267 [↩]
- Waddington, C. H. ‘Genetic Assimilation of an Acquired Character’. Evolution 7, no. 2 (1953): 118–26. https://doi.org/10.1111/j.1558-5646.1953.tb00070.x. [↩]
- Rutherford, S. L., and S. Lindquist. ‘Hsp90 as a Capacitor for Morphological Evolution’. Nature 396, no. 6709 (26 November 1998): 336–42. https://doi.org/10.1038/24550 [↩]
- Jarosz, Daniel F., and Susan Lindquist. ‘Hsp90 and Environmental Stress Transform the Adaptive Value of Natural Genetic Variation’. Science (New York, N.Y.) 330, no. 6012 (24 December 2010): 1820–24. https://doi.org/10.1126/science.1195487 [↩]
- Rohner, Nicolas, Dan F. Jarosz, Johanna E. Kowalko, Masato Yoshizawa, William R. Jeffery, Richard L. Borowsky, Susan Lindquist, and Clifford J. Tabin. ‘Cryptic Variation in Morphological Evolution: HSP90 as a Capacitor for Loss of Eyes in Cavefish’. Science (New York, N.Y.) 342, no. 6164 (13 December 2013): 1372–75. https://doi.org/10.1126/science.1240276. [↩]
- Rutherford, Suzannah, Yoshikazu Hirate, and Billie J. Swalla. ‘The Hsp90 Capacitor, Developmental Remodeling, and Evolution: The Robustness of Gene Networks and the Curious Evolvability of Metamorphosis’. Critical Reviews in Biochemistry and Molecular Biology 42, no. 5 (October 2007): 355–72. https://doi.org/10.1080/10409230701597782. [↩]
- Specchia, Valeria, Lucia Piacentini, Patrizia Tritto, Laura Fanti, Rosalba D’Alessandro, Gioacchino Palumbo, Sergio Pimpinelli, and Maria P. Bozzetti. ‘Hsp90 Prevents Phenotypic Variation by Suppressing the Mutagenic Activity of Transposons’. Nature 463, no. 7281 (4 February 2010): 662–65. https://doi.org/10.1038/nature08739. [↩]