Plasticity-led evolution

I am very interested in plasticity-led evolution; the putative process through which phenotypic plasticity, i.e. the interaction between organism and environment, may facilitate or even direct evolution. While the claim that the environment may influence organismal development, phenotype, behaviour, etc. is hardly controversial, the suggestion that this plasticity may play a central role in evolution is very much so.

Phenotypic plasticity is classically regarded as a trait much like any other that can be selected for or against in terms of sensitivity, magnitude and effect. Yet modern evolutionary theory regards plasticity as a complex higher order feature of an organism; a mechanic that controls the rules by which environment and organism interact. From this theoretical perspective, phenotypic plasticity likely plays a more central role in evolution than merely existing as a trait presented to natural selection.

Fundamental to understanding the process of plasticity-led evolution are the concepts of stabilizing selection, genetic canalization and evolutionary capacitance.

Stabilizing selection, genetic canalization and evolutionary capacitance

Stabilizing selection describes the process by which natural selection selects not only for a phenotypic optimum but also for reduced variation around that optimum. Phenotypic variation decreases as an organism adapts to an environment. However, the manner in which an organism achieves this reduced phenotypic variation may be through reducing the degree to which its genome and development interact with the environment. Development that is thus disconnected from environmental influence is said to be canalized. Genetic canalization can also occur by reducing developmental sensitivity to variability within the genome itself. In both of these cases genetic canalization can be understood as the degree to which development reliably produces the same phenotype.

A key outcome of canalization is the shielding of parts of the genome from natural selection. When environmental interaction with the genome is removed or reduced, or when development is less sensitive to genomic variability, a greater portion of the genome exerts no effect on the phenotype. When this is the case, these parts of the genome can freely accumulate variation over time.

Genetic variation accumulated thus, in shielded parts of the genome not presented to natural selection, is also known as cryptic genetic variation (CGV). Yet canalization is not eternal; extreme environmental factors may overcome canalization and interact with previously shielded parts of the genome. When this occurs, CGV acts as a capacitor suddenly releasing its accumulated variation and consequent variability of phenotype. For this reason, genetic canalization is said to generate evolutionary capacitance over time in the form of CGV.

To recapitulate: during stabilizing selection phenotypic variation decreases around its optimum dictated by natural selection. However, genetic variation actually increases in the form of CGV, which accumulates in a population and which may act as a capacitor facilitating rapid bursts of evolution when released due to extreme environmental stress.

Genetic accommodation and genetic assimilation

The expression of CGV causes a rapid increase in phenotypic variation, as previously shielded genetic material once again becomes involved in development. If some of this uncovered variation increases organismal fitness then the environment can be understood as both inducing as well as selecting for its expression. A process of stabilizing selection can then begin once more as the organism begins to canalize this novel phenotype.

Genetic accommodation is the process in which the environmental regulation of a phenotype undergoes adaptive change. In the context of plasticity-led evolution this occurs when released CGV presents useful variation that can then undergo selection. In this instance, as in the stabilizing selection mentioned above, selection is both for a phenotypic optimum as well as decreased variation around that optimum.

Genetic accommodation can then occur yielding developmental changes such that environmentally induced, previously cryptic variation, become less dependent on the environmental trigger. In other words, the newly uncovered variation becomes increasingly genetically canalized. The extreme process of a previously plastic response becoming completely obligate, regardless of environmental factors, is known as genetic assimilation.

Given this framework, the process of plasticity-led evolution becomes cyclical in nature. Stabilizing selection causes genetic canalization with subsequent accumulation of CGV as a result. Extreme environmental stress causes the release of CGV resulting in a rapid release of phenotypic variation. If some of the released phenotypic variation is beneficial, then stabilizing selection acts on it and the cycle repeats itself.

Quantum evolution and punctuated equilibria

While this process of evolution is a currently controversial hypothesis, it is in fact highly congruent with historical readings of evolution, the fossil record in particular. Indeed it describes, I believe, the same process that Simpson in the 1940s identified as quantum evolution. According to him this constituted a separate “mode” of evolution typified by a “relatively rapid shift of a biotic population in disequilibrium to an equilibrium distinctly unlike an ancestral condition.”

Similarly, Eldredge and Gould’s punctuated equilibria correspond to the process of plasticity-led evolution. Episodes of rapid adaptive evolution facilitated by environmentally induced releases of CGV following periods of environmental stasis and stabilizing selection would generate precisely the evolutionary pattern described above.

So it seems that the fossil record may be useful place to look for evidence of plasticity-led evolution. Paleobiological research aiming to explore this process in the fossil record will require morphometric methods capable of detecting subtle patterns of intra- as well as interspecific variation. However, investigation of the fossil record has historically recorded variation as discrete, which has rendered such analysis problematic.

A central aim of my work is to develop and utilize alternative approaches to understanding the fossil record that instead quantify variation as continuous. In my work with Davidonia, I developed such techniques and in my ongoing work with Agnostus and its relatives I employ them to search the fossil record for evolutionary patterns consistent with the predictions of plasticity-led evolution.

Developmental bias and convergent evolution

If certain parts of the genome or development interact more frequently with the environment than others, then CGV is more likely to accumulate in these periodically shielded parts. This constitutes a developmental bias in making evolution along trajectories governed by these parts more accessible to the organism. In other words, plasticity-led evolution will then favour adaptive change facilitated by particular regions of the genome and development.

Such a bias may prove to be an important causal factor for patterns of convergent evolution across independent lineages during diversification events. I work with the Anolis lizards of the Caribbean and Americas for precisely this reason. The aim of one of my Anolis projects is to investigate patterns of phenotypic plasticity and variation across and between Anolis species in order to understand putative underlying developmental bias and potential plasticity-led evolution directing evolution.