Ledon-Rettig et al. provide a very interesting and lucid discussion of recent studies that show or suggest epigenetically mediated transmission of behavioral variation across generations. They emphasize the potential ecological and evolutionary importance of such effects, and offer advice and encouragement for behavioral ecologists interested in exploring such effects. One aspect of this article that I particularly like is the lack of emphasis on distinguishing effects across one or two generations from effects that potentially span many generations. A pregnant rat (F0) has female embryos (F1) in her womb and, at some point in their development, these embryos have their own germ cells (F2). Thus, an environmental effect experienced by the pregnant rat can be regarded as acting directly on generations F0−F2, and there is a tendency to regard environmental effects that can reach the F3 generation as being in some sense qualitatively different (and perhaps more interesting) than effects limited to F1 or F2. But, although it is indeed interesting to ask why some environmental effects can be transmitted over more generations than others in the absence of the inducing environmental factor, there is no obvious reason to regard more long-term effects as being more important from an ecological or evolutionary perspective. Theoretical analyses have shown that factors that are stably transmitted only across a single generation can affect a population’s prospects for persistence in a changing environment (reviewed in Bonduriansky et al. 2012), as well as influence patterns of selection and alter the course of evolution (Danchin et al. 2011; Day and Bonduriansky 2011; Jablonka and Lamb 2005; Laland 1994). All such effects violate the assumptions of classical population genetics, and thus necessitate a re-examination of evolutionary models (Danchin et al. 2011; Day and Bonduriansky 2011; Jablonka and Lamb 2005). I therefore see no reason to draw a sharp distinction between effects on the basis of the number of generations that they span. Rather, all such effects—the variety of mechanisms and patterns of ancestors’ influence on descendants’ phenotype—can be considered part of an extended concept of heredity. However, epigenetically mediated effects are part of a much broader spectrum of nongenetic effects of ancestors on descendants (Bonduriansky and Day 2009; Danchin et al. 2011; Jablonka and Lamb 2010). Although heritable epigenetic variation is fascinating and may be enormously important, there is no reason to believe that epigenetically mediated effects (in the narrow sense of “transgenerational epigenetic inheritance”) are more interesting, more important, or qualitatively distinct from other types of nongenetic effects (nutrient-mediated, hormone-mediated, learning-mediated, etc.) in their ecological and evolutionary implications. For example, as Ledon-Rettig et al. point out, a rodent can influence the phenotype of its offspring by transmitting an epiallele through the germ-line, or by inducing epigenetic changes in the soma of the offspring. But a rodent might also influence the phenotype of its offspring by providing it with more or less milk and varying the nature and concentration of nutrients, antibodies, and other substances present in the milk, by transferring compounds or microflora in feces that are eaten by the offspring, by performing behaviors that offspring learn to imitate, or by shaping the ambient environment that offspring encounter (see Avital and Jablonka 2000). Ledon-Rettig et al. provide fascinating examples of epigenetically mediated effects and rightly urge behavioral ecologists to investigate such effects. But why should such effects be of greater interest to behavioral ecologists than other kinds of nongenetic effects? Indeed, some of the examples adduced by Ledon-Rettig et al. are not clearly linked to epigenetic mechanisms and, in several cases, are more likely to be mediated by other factors. All mechanisms of nongenetic inheritance appear to share two interesting properties: they can mediate the transmission of environmental influences (“acquired traits”) across generations, and they can “mutate” (or switch between alternative states) at high rates. Consequently, all such mechanisms can amplify heritable phenotypic variation on which selection can act, mediate (mal)adaptive parental effects and, at least in theory, facilitate population persistence in fluctuating or rapidly changing environments and affect the dynamics and course of evolutionary change. Behavioral ecologists (and evolutionary ecologists more generally) should therefore seek to uncover and understand the implications of all nongenetic mechanisms of inheritance. Although the proximate basis of the effects is an interesting subject of study, and may influence the stability and patterns of transmission of the effects, there is no obvious reason to regard one mechanism as more important and more worthy of study than the rest.
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Oct 3, 2023
Christelle Hennequet-Antier + 9
