Three epigenetic information channels and their different roles in evolution

Abstract

There is increasing evidence for epigenetically mediated transgenerational inheritance across taxa. However, the evolutionary implications of such alternative mechanisms of inheritance remain unclear. Herein, we show that epigenetic mechanisms can serve two fundamentally different functions in transgenerational inheritance: (i) selection-based effects, which carry adaptive information in virtue of selection over many generations of reliable transmission; and (ii) detection-based effects, which are a transgenerational form of adaptive phenotypic plasticity. The two functions interact differently with a third form of epigenetic information transmission, namely information about cell state transmitted for somatic cell heredity in multicellular organisms. Selection-based epigenetic information is more likely to conflict with somatic cell inheritance than is detection-based epigenetic information. Consequently, the evolutionary implications of epigenetic mechanisms are different for unicellular and multicellular organisms, which underscores the conceptual and empirical importance of distinguishing between these two different forms of transgenerational epigenetic effect.

Reduced fitness in progeny from old parents in a natural population

“…First described by Alexander Graham Bell (1), this negative influence of parental age on offspring fitness [known as the "Lansing effect" (2-6)] has been observed in humans and in many taxa in the laboratory. Such transgenerational effects might have an epigenetic cause and are critical for understanding the evolution of late reproduction and longevity (7)(8)(9)(10)(11). However, to our knowledge, an effect of parental age on fitness in the next generation has not yet been shown conclusively in the wild, perhaps because its detection requires an exact knowledge of parental age and of the lifetime fate of offspring, data that are difficult to gather in natural populations (12).…”

When is incomplete epigenetic resetting in germ cells favoured by natural selection?

“…This is the approach we take in this paper (see also [24,[38][39][40]). Specifically, we develop a simple model of an asexual organism with a single period of epigenetic resetting during germ cell formation.…”

“…Is incomplete epigenetic resetting an occasional phenomenon with neutral or negative effects on fitness, or can incomplete resetting be an adaptation [17,[20][21][22][23][24][25][26]? The consequence of incomplete epigenetic resetting in germ cells is that environmental conditions encountered in one generation can have effects on the development of the next generation or even many generations later.…”

Predator-induced phenotypic plasticity within- and across-generations: a challenge for theory?

“…[17][18][19]). Transgenerational responses are expected to be favoured when there is environmental heterogeneity across generations and when offspring environmental conditions are predictable from parental environmental conditions [2,3,[20][21][22]. Current theory that explicitly incorporates phenotypic plasticity and 'maternal effects' [23,24] indicates that predictable environmental variation will simultaneously select for increased plasticity within-and across-generations.…”