Phenotypic plasticity – contrasting species-specific traits induced by identical environmental constraints

Can it be assumed that a specific environmental constraint imposed on different species leads to a convergence in, for example, morphology? A phenotype expressed in response to external stimuli (e.g. size-reduction in response to mechanical stress) should be adaptive regardless of species – this is largely intuitive, but has been poorly studied. In this issue (pp. 651–660), Puijalon & Bornette reveal exciting new data that suggest that phenotypic plastic responses to identical environmental constraints may indeed be species-specific (Puijalon & Bornette, 2004).

Phenotypic plasticity – background

Early twentieth century research on phenotypic plasticity has been largely overlooked, with some exceptions (e.g. Bradshaw, 1965), until the last few decades. Not until recently has the concept of phenotypic plasticity become an important and integrated part of modern evolutionary and ecological research (Pigliucci, 1996; see Box 1). The past few decades have seen a large amount of interdisciplinary research being carried out on various aspects of phenotypic plasticity and reaction norms (e.g. Moran, 1992; Dudley & Schmitt, 1996; Lachmann & Lablonka, 1996; Preston, 1999; Pigliucci, 2002), together with a number of reviews (e.g. Coleman et al., 1994; DeWitt et al., 1998). Debates have also focused on evolution of phenotypic plasticity, including traits, models and gene expression (see De Jong, 1995 for an overview). Today, it seems clear that phenotypic plasticity must be recognised as central to evolution rather than a minor phenomenon, secondary to ‘real’ genetic adaptation (Sultan, 1992).

Table 1. 

Box 1. What is phenotypic plasticity?

Phenotypic plasticity is the ability of individual genotypes to express diverse phenotypes, by altering, for example, morphology or physiology, in response to changes in environmental conditions (Schlichting, 1986; Bradshaw, 1965; Stearns, 1989; Schlichting & Pigliucci, 1998). The function or relationship that describes the phenotypes produced by a given genotype when exposed to a certain range of environments is called the reaction norm (Pigliucci, 1996). The reaction norm can be viewed graphically in a phenotype-environment space (Fig. 1) or as an equation: VP = VG + VE+VGxE+Verr. VP is the total phenotypic variation of a trait, VG is the genetic variance, VE is the environmental variance, VGxE is the genotype–environmental interaction variance, and Verr is the residual error variance. The reaction norm is what is actually inherited (i.e. the ability to express different phenotypes). However, it has been pointed out that plasticity can also be produced by allelic effects that vary across environments (Via, 1993).

Figure 1. Conceptual graphic presentation of reaction norms (phenotypic expressions across environments for different genotypes or species). Bold letters (G, E, GxE) indicate significant genetic, environmental, or gene–environment interaction variance. (a) No phenotypic plasticity (denoted by flat reaction norms) but with significant genetic effects (space between genotypes). (b) Plasticity and genetic variation for traits (sloped and separated reaction norms), but no interaction variance (parallel slopes). (c) Differently sloped (positive) interaction norms indicating genetic variation for plasticity (genotype–environmental interaction). (d) Differently sloped interaction norms (both positive and negative) indicating genetic variation for plasticity. Opposite slopes indicating that the phenotypic expression across the environmental gradient goes in different directions depending on genotype (or species). Figure and text partly modified from Schlichting & Pigliucci (1998) and DeWitt & Scheiner (2004).

Current research

An interesting aspect of ongoing research is a closer coupling between genetics and ecologists (e.g. Jasienski et al., 1997), where molecular evolutionary geneticists work together with plant ecologists. This is likely to be a fruitful cross-pollination that will reduce the risks of research ‘inbreeding’ and increase the development of healthy new insights in complex and dynamic ecological systems. It is unfortunate if genetic and functional aspects of plasticity are studied separately: they should be complementary.

In addition to investigating the genetic and evolutionary basis for, and effects of, phenotypic plasticity, it might be viewed in the context of species interactions, plant community structure and food-web dynamics. Reciprocal phenotypic change between individuals of interacting species (Agrawal, 2001) is an area of research that should lead to a greater understanding, not only of phenotypic plasticity, but also of species interactions and how these are affected by, and affect, the environment. The new findings of Puijalon & Bornette should stimulate research on the significance of species-specific plastic responses and how these affect distribution and abundance of individuals and species. It is possible that different species have different ‘starting points’ (i.e. genetic conditions), leading to different expressions of adaptive plasticity in traits in a given environment. Reduction in stem length as a response to increased flow velocity might be adaptive. But if the species is genetically limited in this aspect (i.e. does not have the ability to effect plasticity in stem length) it is likely that an alternative response (e.g. decreased rigidity) might also be adaptive. In a competition situation the magnitude and cost of plasticity might be factors that decide the outcome.

Aquatic macrophytes are likely to be a good group of plant to focus on considering their evolutionary history with several distantly related taxa, exposed to several specific environmental constraints caused by adaptations to aquatic life. It is possible that inherent phenotypic plasticity might be a major factor explaining observed distribution patterns and shifts in dominance between species.

An applied aspect of plasticity research is the question as to why some species are invasive and others not. It has been suggested that invasive species are invasive just because they are more plastic (Agrawal, 2001). Again, aquatic plants are relevant since invasive species are frequent in aquatic habitats and often outcompete the native flora in lakes and rivers (e.g. Elodea canadensis in Europe, Myriophyllum spicatum in North America and Salvinia spp. and Eichornica crassipes in large parts of the tropics). From a nature conservation point of view, a better understanding about the ecology of invasive species is paramount, including the species-specific phenotypic plasticity.

Finally it is important to note that many phenotypic traits of plants change dramatically over the course of plant growth – a phenomenon termed ontogenetic drift (Evans, 1972). Therefore any studies concerning phenotypic plasticity must take into account size-dependent variation, in order not to confuse this with true phenotypic plasticity. The interpretation of variation in many phenotypic traits will therefore depend on whether comparisons are made as a function of plant age, size or developmental stage (Coleman et al., 1994). Allometric studies where difference in size is accounted for is necessary for the correct interpretation of results concerning phenotypic plasticity (Schlichting & Pigliucci, 1998).

Perspectives

The work of Puijalon & Bornette opens up new, interesting areas of research, including further studies on difference in plastic responses between species, but also, for example, differences in responses between life-history stages (both within and between species), and how this might affect competition and plant community structure and dynamics. A first step should be further studies to examine whether different responses to an environmental change between species are in fact adaptive in both cases (i.e. can different and even opposite trait responses increase fitness in different species under a given set of external stimuli?). Proof of adaptive plasticity also requires analysis of fitness in multiple environments.