# Transgenerational plasticity and adaptation

Phenotypic plasticity can occur both within and across generations. It is defined as within-generation plasticity if it occurs within a single generation: an individual encounters distinct environments and reacts accordingly. Conversely, transgenerational plasticity includes heritable phenotypic responses that persist for multiple generations, in which the conditions experienced in one generation can interact with conditions experienced by subsequent generations (Agrawal et al., 1999; Salinas et al., 2013). It is essential to point out that some authors distinguish even further between "intergenerational" and "transgenerational" plastic responses. Intergenerational responses (or parental effects) refer to phenomena spanning short timescales (i.e. one generation after the initial trigger) (reviewed in: Badyaev & Uller, 2009). Transgenerational effects refer to phenomena persisting for multiple generations in the absence of the initial trigger and thus cannot be ascribed to direct effects of the trigger. For simplicity reasons, in this chapter, we will use the broad definition of "transgenerational" to encompass both of these sub-categories. Furthermore, when not specified either “within-generation” or “transgenerational, we will refer to the broad definition of “transgenerational” plasticity.

Intuitively, one could think that similar conditions cause the expression of analogous within-generation and transgenerational phenotypic responses. However, simulation models suggest a different scenario. Natural selection may act on them independently. In particular, within-generation plasticity seems to be favored in an environment characterized by high temporal variability. In contrast, transgenerational responses are favored when the offspring environment is predictable across generations, showing low temporal variability and a slow rate of environmental change (Leimar and McNamara, 2015). That such environmental conditions exist in nature was recently demonstrated using 120 years of climate records for the United States of America (Colicchio and Herman, 2020). However, selection can also favor transgenerational plasticity in highly variable environments (Lampei et al., 2017). It all depends on the environmental correlations between the parental and the offspring generation. This correlation can have the form of a temporal autocorrelation in, e.g. temperatures (Leimar and McNamara, 2015; Colicchio and Herman, 2020) or a correlation between different environmental variables so that, e.g. the amount of rain in the parental season affects the density of seedlings in the offspring season (Lampei et al., 2017).

In particular, transgenerational plasticity can be adaptive, maladaptive or neutral. Transgenerational plasticity is neutral when the parental environment has no effects on the fitness of the offspring, and it is maladaptive when the parental environment limits the fitness of the offspring (Sultan, 1996; Roach and Wulff, 1987; Galloway, 1995; Donohue and Schmitt, 1998). Transgenerational plasticity is adaptive when the parental environment increases the fitness of the offspring, or in other words, when the parental environment allows the plants to pre-adapt their offspring to the conditions they will experience.

For example, Whittle et al. (2009) reported evidence for adaptive transgenerational responses to heat stress in A. thaliana that persisted over at least two generations. Using a set of homozygous inbred lines, they exposed the F0 and F1 generations to heat stress (30°C), and they found that the F3 progeny increased the reproductive output fivefold under heat stress. This effect persisted into the F3 generation, even when F2 plants were grown at a moderate temperature (23°C) (Whittle et al., 2009). The specific mechanisms leading to this fitness increase in the offspring were, however, not documented. The effects of temperature stress also appear to be heritable and potentially adaptive in the cosmopolitan weed Plantago lanceolata. Case et al. (1996) showed that the effects of cold temperature treatment persisted across two generations, significantly enhancing seed weight and fitness-related leaf and life-history traits in adult grandchild plants. Contrary to what was often assumed, this result clearly showed that transgenerational effects might not be confined to the seedling stage. Furthermore, in this species, the paternal temperature also significantly affected offspring traits via interactions with the maternal temperature environment (Lacey, 1996). Furthermore, the paternal environment may also be relevant in outcrossing species, though less than the maternal environment (Roach and Wulff, 1987; Mazer and Gorchov, 1996; Diggle et al., 2010).

Beyond temperature, also other environmental variables can trigger adaptive transgenerational plasticity. In P. lanceolata, offspring showed improved relative fitness when exposed to maternal nutrient availability (Latzel et al., 2014). In Mimulus guttatus, parental wounding induced resistance against natural herbivory (Colicchio, 2017). Also known for strong adaptive parental effects is the maternal shading status that prepares offspring of several herbs for growing in the open (sun) or under canopy (shade) (Galloway and Etterson, 2007; McIntyre and Strauss, 2014). So, despite the rather specific nature of environments that favor transgenerational plasticity, it appears to be frequently found among plants. However, this seems to depend on life history. In a recent meta-study, transgenerational plasticity was frequent and adaptive among annual plants but less frequent and neutral or negative among perennial plants (Yin et al., 2019).

Transgenerational effects are also genotype‐specific as seed families differed in transgenerational plasticity (Alexander and Wulff, 1985; Schmitt et al., 1992; Schmid and Dolt, 1994; Andalo et al., 1998; Agrawal, 2001, 2002; Riginos et al., 2007; Bossdorf et al., 2009). More recently, these differences were used to demonstrate that the reaction norm of parental effects can correlate with climate variables (Groot et al., 2016). In other words, the differences between genotypes in transgenerational plasticity seem to occur not at random but were likely favored by past selection.

To conclude, we do have evidence from different sources that transgenerational plasticity contributes to plant adaptation. However, for a more comprehensive overview, we need more examples, especially studies that include many genotypes or many species, to increase the generality of conclusions.
