Induction of subindividual variation: a commentary on ‘Intra-individual variation in Galium odoratum is affected by experimental drought and shading’

Variability is a ubiquitous characteristic of biological systems, occurring at all levels of spatial organization from biomes to individual organisms. In modular organisms such as plants, the reiteration of structures such as leaves, fruits or flowers confers the potential for an enormous trait variation within individuals; this level of variation is referred to as subindividual variation (Herrera, 2017). As an example, a plant can present leaves with different size, colour and shape, such as the prickly and smooth-edged leaves found within a holly tree (Ilex aquifolium). Such trait diversity arises due to phenotypic plasticity at the organ level (subindividual plasticity); each organ is a rerun of the same genotype under different microenvironmental circumstances, and so, like other levels of plasticity, subindividual plasticity often has an epigenetic basis (Herrera, 2017).

Subindividual plasticity allows trait variation to originate within individual genotypes. This subindividual trait variation can be larger than among-individual or population-level variation and constitutes a major source of phenotypic variation in nature (Herrera, 2017). However, most studies of trait adaptation to climate change have focused on individual genotypes (Exposito-Alonso et al., 2019), and the potential adaptive value of subindividual plasticity remains unknown. Given thst subindividual variation accounts for a large part of natural diversity, and due to the importance of biodiversity for ecosystem functioning and mitigation of anthropogenic change, exploring the evolutionary and ecological causes and consequences of subindividual variation is a major scientific and societal challenge. This avenue of thinking represents a new perspective from which to explore and understand evolutionary processes and the consequences of biological diversity across scales of organization.

In this issue of Annals of Botany, Møller et al. (2023) explore plant responses to environmental change at different levels of organization – with a particular focus on the subindividual level – through an experimental approach using clones of Galium odoratum. Their work analyses how subindividual variation in ramet height and leaf length and width is modified by experimental drought and shade and whether it differs among populations of origin. To do so, they used a novel experimental design. Genetic individuals (genets) were sampled from 21 populations in three regions, and within each genet, four genetically identical ramets were subject to shade and drought treatments in a common garden. This allowed them to study constitutive (control treatments) and induced trait variation (experimental treatments) at different hierarchical levels of organization, which they describe as intra-population, intra-genet, intra-ramet and intra-shoot levels.

Møller et al. found first that most of the trait variation occurred within genotypes and thus at the subindividual level independent of genetic variation. Furthermore, they found that the degree of subindividual variation, quantified as the coefficient of variation (CV), varied between individual genotypes: the subindividual CV of plant height was lower for genotypes from environments with lower soil temperatures, which they suggest may be an adaptive response. Second, they found that subindividual trait variation responded to the current environment and is therefore inducible. Shade led to increased subindividual CV of leaf length, while drought reduced the CV of leaf width. These effects could be interpreted as subindividual adjustments of the phenotype to optimize use of resources and organismal fitness. Importantly, despite the response of the CV, average trait values did not change with experimental treatments. This indicates that trait variation can be more significant for organismal fitness and rapid adjustment to the environment than the average values of traits expressed. Finally, that the relationship between the average and variation of traits within individual genotypes responded to the current environment implies that the environment can directly shape the relationship between genetic and environmental drivers of phenotypic diversity. At least one study has previously approached these questions, finding as well that subindividual variation responds to the environment (Sobral et al., 2019). However, the work of Møller and colleagues is much more conclusive because the use of a clonal plant allowed them to control for the effects of genetic diversity when studying environmental effects on subindividual plasticity. In addition, imposing environmental treatments on genetically identical organisms allowed them to explore the inducibility of plasticity in trait CVs at different subindividual levels of organization.

One approach unexplored by Møller et al. is the use of genetic analyses to test genetic uniformity within clones, and so rule out the existence of genetic mosaics. Nevertheless, their results provide a valuable basis for further progress along a couple of critical avenues of research. First, given that they found environmental induction of levels of subindividual variation, the next step would be to investigate subindividual plasticity across generations (Fig. 1). With respect to transgenerational effects, we know now that epigenetic variation can be induced by a host of natural environmental triggers, affecting multiple ecologically relevant traits, and respond to environmental change across generations (Sobral and Sampedro, 2022). Furthermore, epigenetic mosaics within plant individuals can drive variation in fitness-related traits of offspring (Herrera et al., 2022). In the system investigated by Møller et al., subindividual epigenetic variation probably provides the mechanistic basis for subindividual trait variation, and so we may expect that the induction of subindividual variation by the environment they found might also have transgenerational effects. Transgenerational subindividual plasticity could vary the temporal and spatial organization of trait diversity available for natural selection to act on, changing the evolutionary dynamics of populations (Sobral et al., 2021). Thus, an emerging priority is to investigate the transgenerational inheritance of subindividual trait and epigenetic variation (Fig. 1).

Fig. 1.

Subindividual variation can be affected by environmental effects as found by Møller and colleagues. The next step in the research agenda is to investigate if this induction can be transgenerational. If it is, we could expect to meet the prediction in this graph. Four individuals of Galium odoratum related by ancestry across four generations are represented. Shade (crossed out sun icon) effects across generations could theoretically be related to transgenerational induction on subindividual trait and epigenetic variation. Transgenerational induction of subindividual variation would increase phenotypic diversity in nature, with manifold evolutionary and ecological implications.

Second, subindividual variation has been shown to be advantageous to individual plants by enhancing whole-plant photosynthetic performance through improved water economy and/or carbon assimilation (Herrera et al., 2015). Thus, how subindividual plasticity and function scale up to impact ecosystem functioning is another area ripe for investigation. For example, both species richness and trait diversity affect the ability of ecosystems to fix carbon dioxide from the atmosphere, and to store organic carbon in soils, given the complementary functional effects between species or individuals with different traits (Westerbrand et al., 2021). Epigenetic diversity, as an underlying mechanism behind trait plasticity, has also been shown to be linked to ecosystem processes, such as biomass production or litter decomposition (Puy et al., 2021). Yet, although subindividual variation is one of the largest components of plant trait variation in nature (Herrera, 2017), no studies have investigated whether trait and epigenetic diversity within individual plant genotypes can scale up to impact ecosystem function. Testing effects of subindividual variation on carbon atmospheric uptake, soil carbon storage and water fluxes would fill a major gap in our understanding of the relationships between diversity and ecosystem functioning in a changing world. Seen from this perspective, the work of Møller et al. provides a welcome step towards the goal of integrating subindividual trait diversity into both evolutionary and global change research.