Transgenerational Plasticity: A Third Way of Adapting to Climate Change
Salinas, S. and Munch, S.B. 2012. Thermal legacies: transgenerational effects of temperature on growth in a vertebrate. Ecology Letters 15: 159-163.
This phenomenon, as they describe it, "occurs when the environment experienced by the parents prior to fertilization directly translates, without DNA sequence alteration, into significant changes in the shape of offspring reaction norms (Fox and Mousseau, 1998), resulting in a significant interaction between parental and offspring environment effects."
Such effects have been observed in many traits of several species; yet they note that "TGP in thermal growth physiology has never been demonstrated for vertebrates," which is consequently what they set out to do for sheepshead minnows (Cyprinodon variegatus), a small fish that is common to nearshore marine and estuarine waters along the east coast of the United States and throughout the Caribbean.
Working with fish they had raised from the egg stage to adults in aquaria they had maintained at constant temperatures of either 24, 29 or 34°C, Salinas and Munch allowed the soon-to-become parent fish to spawn, after which they collected the newly fertilized eggs from each of the three temperature treatments and allowed a third of each group to develop within each of a new set of aquaria maintained at the same three standard temperatures, during which time the growth rates of the new sets of juveniles were determined.
So what did they learn?
The two researchers report that offspring from high (34°C) and low (24°C) temperature-raised parents grew best at high and low temperature, respectively, "suggesting an adaptive response," with growth rates differing by as much as 32% (0.60 vs. 0.46 mm/day, when both sets of offspring were maintained at 34°C). And in discussing this result, Salinas and Munch say that the rate of adaptive response change that they observed "is roughly two orders of magnitude greater than the median rate of phenotypic change found in a review of the subject (Hendry and Kinnison, 1999)."
In terms of the range of applicability of the TGP phenomenon, the two scientists say that it has so far "only been demonstrated for milkweed bugs (Groeters and Dingle, 1988), butterflies (Steigenga and Fischer, 2007), and thale cress (Blodner et al., 2007; Whittle et al., 2009)," but they note that "in all cases, offspring growth is maximized at the temperature experienced by the parents."
As for the importance of TGP, Salinas and Munch write that it "may allow for a rapid response to environmental changes," citing Bossdorf et al. (2008), while specifically noting that "changes in precipitation may be counteracted via TGP in desiccation tolerance in invertebrates (Yoder et al., 2006) or drought tolerance in plants (Sultan et al., 2009)," and more especially noting that "higher CO2 concentrations have been shown to elicit a TGP response in three plant species (Lau et al., 2008) and to alter predator-induced TGP responses in aphids (Mondor et al., 2004)."
All in all, therefore, Salinas and Munch say of this exciting new "area of active current research" that it "may qualitatively change projections for extinction risk and other climate impacts" ... and, as might be added, change them for the better.
Blodner, C., Goebel, C., Feussner, I., Gatz, C. and Polle, A. 2007. Warm and cold parental reproductive environments affect seed properties, fitness, and cold responsiveness in Arabidopsis thaliana progenies. Plant, Cell, and Environment 30: 165-175.
Bossdorf, O., Richards, C.L. and Pigliucci, M. 2008. Epigenetics for ecologists. Ecology Letters 11: 106-115.
Fox, C.W. and Mousseau, T.A. 1998. Maternal effects as adaptations for transgenerational phenotypic plasticity in insects. In: Mousseau, T.A. and Fox, C.W. (Eds.). Maternal Effects as Adaptations. Oxford University Press, New York, New York, USA, pp. 159-177.
Groeters, F.R. and Dingle, H. 1988. Genetic and maternal influences on life history plasticity in milkweed bugs (Oncopeltus): response to temperature. Journal of Evolutionary Biology 1: 317-333.
Hendry, A.P. and Kinnison, M.T. 1999. The pace of modern life: measuring rates of contemporary microevolution. Evolution 53: 1637-1653.
Mondor, E.B., Tremblay, M.N. and Lindroth, R.L. 2004. Transgenerational phenotypic plasticity under future atmospheric conditions. Ecology Letters 7: 941-946.
Steigenga, M.J. and Fischer, K. 2007. Within- and between-generation effects of temperature on life-history traits in a butterfly. Journal of Thermal Biology 32: 396-405.
Sultan, S.E., Barton, K. and Wilczek, A.M. 2009. Contrasting patterns of transgenerational plasticity in ecologically distinct congeners. Ecology 90: 1831-1839.
Whittle, C.A., Otto, S.P., Johnston, M.O. and Krochko, J.E. 2009. Adaptive epigenetic memory of ancestral temperature regime in Arabidopsis thaliana. Botany 87: 650-657.
Yoder, J.A., Tank, J.L. and Rellinger, E.J. 2006. Evidence of a maternal effect that protects against water stress in larvae of the American dog tick, Dermacentor variabilis (Acari: Ixodidae). Journal of Insect Physiology 52: 1034-1042.