Introduction: What is phenotypic plasticity?

The study and understanding of phenotypic plasticity require a multidisciplinary approach, including different areas of biology, such as molecular biology, ecology and evolutionary biology. From one side, the multifaceted nature of phenotypic plasticity justifies its attraction; from the other side, it explains the difficulty to unravel a plastic phenotype in toto. In fact, the ecological and evolutionary role of phenotypic plasticity, as well as the molecular mechanisms regulating its responses, are still relatively unknown.

This chapter provides insight into the current state of knowledge of phenotypic plasticity ranging from its historical definition, passing through the known molecular mechanisms and transgenerational responses, and concluding with the possible role of phenotypic plasticity in evolution and adaptation. These concepts are explained using real examples, emphasizing the importance of epigenetic mechanisms as a key regulator of these responses.

a. Historical insights

Phenotypic plasticity started to gain the interest of the scientific community at the beginning of the 20th century. In 1909, Richard Woltereck performed the first experiments on plastic characters and coined the term "reaction norm" to describe the relationship between the expressions of phenotypic traits across a range of different environments (Schlichting and Pigliucci, 1998). Johannsen (1911) was then the first to distinguish between genotype and phenotype, introducing the concept of genotype-environment interaction, which was developed further by the British developmental biologist Waddington. In particular, Waddington introduced the concept of genetic assimilation, which is how a phenotype initially produced in response to an environmental alteration becomes later genetically encoded (Waddington, 1961). Such a process was identified by studying the phenotypes displayed by Drosophila pupae exposed to environmental stresses (i.e. heat shock or ether vapor) (Waddington, 1953; Waddington, 1956). These phenotypes were indeed initially induced by environmental stress and became then genetically fixed, i.e. they were expressed even without environmental induction. Since these phenotypes were not innate but induced by an environmental event, Waddington argued that genetic assimilation was a change in the pathways of the developmental program due to an environmental change. He claimed that phenotypes result from the interaction between genes and often environment-sensitive developmental factors, which he called for the first time epigenetic factors (Waddington, 1957).

Another conceptual advancement for plasticity research came in 1965 when Anthony Bradshaw suggested that plastic traits may be influenced by natural selection (Bradshaw, 1965). According to his model, plastic traits are environmentally induced and genetically controlled, so that selection can directly act on them. The link between plasticity and evolution was then further developed by Mary-Jane West-Eberhard. She proposed that the genetic accommodation of environmentally induced phenotypes can lead to morphological or behavioral diversification in animals and plants, arguing that phenotypic plasticity plays a crucial role in evolution and speciation (West-Eberhard, 2005).

b. Current understanding in plants

Phenotypic plasticity is today described as the ability of one genotype to produce more phenotypes when exposed to different environments (Pigliucci, 1997). Phenotypic plasticity includes all types of environmentally induced changes, such as physiological, morphological and life-historical traits. Even though it is common in all organisms, plasticity is more broadly expressed in plants, which cannot move away from unfavorable environments because of their sessile nature.

The relationship between phenotype and environment is often represented by a reaction norm (Stearns, 1992; Roff, 1997). In other words, the reaction norm shows the range of phenotypes that a single genotype can express across a range of environments. The reaction norm for any specific trait of a genotype can be visualized as a line or a curve on a two-dimensional plot of the environmental factor (x-axis) versus the phenotype/trait (y-axis) (Fig. 1). The reaction norm is linear when representing two distinct environmental states (e.g. two different temperatures) (Fig. 1A, 2B), while it is linear or non-linear when representing more than two environmental states (e.g. a whole range of temperatures) (Fig. 1D).

The slope of the reaction norm gives hints on the estimation of phenotypic plasticity: a positive (Fig. 1A) or a negative slope (Fig. 1B) implies that the genotype is phenotypically plastic, whereas a flat reaction norm with slope zero represents a non-phenotypically plastic genotype (Fig. 1C).

Figure 1: reaction norms of a single genotype. (A, B, C) Linear reaction norms with positive (A), negative (B) or flat (C) slopes. The positive or negative slopes indicate a phenotypically plastic genotype, while the flat slope a non-phenotypically plastic genotype. (D) Non-linear reaction norm representing more than two environmental states.

Reaction norms representing different genotypes can also be plotted on the same graph, which allows comparing the responses of different genotypes to the same environmental states (Fig. 2). If the two reaction norms are congruent, the two genotypes respond phenotypically in the same way when exposed to the same range of environments (Fig. 2A). When the two reaction norms have identical slope and shape and are shifted along the y-axis, the genotypes show phenotypes that differ on average, but the phenotypic response to the environment is the same (Fig. 2B). When the reaction norms are non-parallel, the two genotypes differ in their phenotypic response to the environment (Fig. 2C-E). Different genotypes of the same species showing non-parallel reaction norms indicate the presence of genotype-by-environment interactions.

Figure 2: reaction norms of two genotypes. (A) Congruent reaction norms indicate that two genotypes display the same phenotypic responses when exposed to the same environments. (B) Reaction norms with identical slope and shape but shifted along the y-axis show genotypes with different phenotypes on average. (C-E) Non-parallel reaction norms indicate that the two genotypes respond phenotypically differently to the same environments.

The sources of phenotypic variation within a population grown in different environments can be summarised by the following equation:

VP = VG + VE + VGxE + Vε.

Here VP is the total phenotypic variance in a trait, VG is the phenotypic variance attributed to differences between the genotypes, VE is the phenotypic variance attributed to differences between the environments, VGxE is the phenotypic variance attributed to the genotype-by-environment interaction, and Vε is the residual or error variance not explained by any of the other sources of variation (Scheiner and Goodnight, 1984).

Notably, each component of this equation can be influenced by epigenetic processes (Banta and Richards, 2018). Epigenetic processes can alter gene expression, ultimately shaping phenotypic variation in response to the environment (Duncan et al., 2014). However, phenotypic responses can also be mediated by indirect physiological and developmental events, such as biochemical mechanisms (reviewed in Kelly et al., 2012), not all of which involve epigenetic processes. For example, extreme temperatures or poor nutrition can directly alter cellular and developmental processes that may also influence complex phenotypic traits.

In summary, phenotypic plasticity arises from diverse mechanisms that can act together, resulting in a wide range of different phenotypes. Although phenotypic plasticity can potentially result also from epigenetic-independent biochemical and nutrient constraints, epigenetic mechanisms can still have a crucial role in mediating many phenotypic responses.