Biological Prescience: The Role of Anticipation in Organismal Processes

Abstract

Anticipation is the act of using information about the past and present to make predictions about future scenarios. As a concept, it is predominantly associated with the psychology of the human mind; however, there is accumulating evidence that diverse taxa without complex neural systems, and even biochemical networks themselves, can respond to perceived future conditions. Although anticipatory processes, such as circadian rhythms, stress priming, and cephalic responses, have been extensively studied over the last three centuries, newer research on anticipatory genetic networks in microbial species shows that anticipatory processes are widespread, evolutionarily old, and not simply reserved for neurological complex organisms. Overall, data suggest that anticipatory responses represent a unique type of biological processes that can be distinguished based on their organizational properties and mechanisms. Unfortunately, an empirically based biologically explicit framework for describing anticipatory processes does not currently exist. This review attempts to fill this void by discussing the existing examples of anticipatory processes in non-cognitive organisms, providing potential criteria for defining anticipatory processes, as well as their putative mechanisms, and drawing attention to the often-overlooked role of anticipation in the evolution of physiological systems. Ultimately, a case is made for incorporating an anticipatory framework into the existing physiological paradigm to advance our understanding of complex biological processes.

Keywords: allostasis; cephalic responses; feed-forward control; microbe; non-cognitive; physiological regulation; prediction.

Figure 1

Example showing the time course of a hypothetical environmental factor (A), the time course of two signals that are correlated with this variable (B), and a demonstration of how the temporal relationship between the environmental variable, signal, and response can be used to distinguish between reactive and anticipatory processes (C).

Figure 2

Anticipatory regulation of sugar metabolism in Escherichia coli. The movement of E. coli from the proximal end of the small intestine toward the distal end is associated with a predictable sequence of exposure, first to lactose followed by maltose (A). Expression of the lac operon occurs in a reactive manner once lactose is present, while the expression of specific maltase genes exhibits anticipatory regulation. Maltase genes are upregulated in the presence of maltose but also significantly expressed upon exposure to lactose in the absence of maltose (B). This regulatory structure induces maltase production in anticipation of future maltose availability and is associated with increased fitness. The data shown here are from Mitchell et al. (2009). Only the expression specific promoters were measured (data for lacY and lacA and only five of the 10 maltase gene promoters are shown).

Figure 3

Diagram showing the key events in a reactive response and a generalized anticipatory response, including the manifestation of error, the initiation of the preparatory phase, downstream reactions, and commencement. Notice that although the duration of each response (D_r and D_a) is the same, the anticipatory response has a shorter response time (RT_a) than the reaction response (RT_r) due to the initiation of the preparatory phase occurring before the manifestation of error.

Figure 4

Summary of key criteria for biological anticipation at different levels of organization, including causal, ecological, physiological, and biochemical considerations.

Figure 5

Graphical representation of the different types of anticipatory processes. (A) Shows how circadian rhythms can regulate the timing of physiological processes in an anticipatory manner. This figure is adapted from Millar and Kay (1996) and shows the upregulation of chlorophyll a/b-binding protein (CAB) expression in Arabidopsis seedlings before the morning increase in light availability. (B) Shows asymmetrical anticipatory regulation (AAR), which occurs when a response is regulated by a stimulus that is correlated with but predates an environmental variable, allowing the response to be carried out in anticipation of the environmental change. (C) Shows priming in a plant-insect model system, where previously attacked, or primed, plants are more resistant than naïve plants to future attack. (D) Shows the J-response curve characteristic in hormesis, where an over-response to a specific stressor can provide beneficial protection from other more general stressors. (E) Demonstrates how parental expressional states can be passed on to offspring to increase fitness in predicted future conditions via transgenerational effects, shown here by heritable gene methylation and histone modifications.