An Integrative Framework for Understanding the Mechanisms and Multigenerational Consequences of Transgenerational Plasticity

Abstract

Transgenerational plasticity (TGP) occurs when the environment experienced by a parent influences the development of their offspring. In this article, we develop a framework for understanding the mechanisms and multi-generational consequences of TGP. First, we conceptualize the mechanisms of TGP in the context of communication between parents (senders) and offspring (receivers) by dissecting the steps between an environmental cue received by a parent and its resulting effects on the phenotype of one or more future generations. Breaking down the problem in this way highlights the diversity of mechanisms likely to be involved in the process. Second, we review the literature on multigenerational effects and find that the documented patterns across generations are diverse. We categorize different multigenerational patterns and explore the proximate and ultimate mechanisms that can generate them. Throughout, we highlight opportunities for future work in this dynamic and integrative area of study.

Keywords: behavioral development; biological embedding; epigenetics; maternal effects; nongenetic inheritance; parental effects; phenotypic plasticity.

Figure 1

Conceptual framework for understanding the steps of transgenerational plasticity. Parents ① detect an environmental cue, to produce ② process the information provided by it, and ③ then use this information and transmit a cue to offspring. Then, their offspring ④ detect and ⑤ process the information in this cue and ⑥ use this information to affect their phenotype. ⑦ Offspring may or may not produce and transmit a cue to grandoffspring, etc.

Figure 2

Potential multigenerational outcomes of a cue experienced in the F0 generation. We assume that the F0 generation is exposed to an environmental cue. (a) The phenotype of the F1 generation is influenced by the cue experienced in the F0 generation, but the effects do not persist into the F2—i.e., the phenotype bounces back. (b) The phenotype of the F1 and F2 generations is influenced by the cue experienced in the F0 generation, but the mean effects weaken between the F1 and F2 generations (for further complexities, see text). (c) The phenotypes of the F1 and F2 generation are similarly influenced by the cue experienced in the F0 generation—i.e., the induced phenotype persists. (d) The phenotype of the F3 generation exceeds the mean of the phenotype induced in the F2 generation, which exceeds the phenotype of the F1 generation—i.e., the induced phenotype accumulates. (e) The phenotype of the F2 generation is influenced by the cue experienced in the F0 generation, but the phenotype of the F1 generation is not—i.e., it is delayed. (f) The phenotypes of the F1 and F2 change in opposite directions in response to a cue experienced in the F0 generation—i.e., they are reversed. Here, we have depicted scenarios in which the mean phenotype increases in response to parental cues, but the direction is arbitrary.