Reflections on the Predictability of Evolution: Toward a Conceptual Framework

Abstract

Evolution is generally considered to be unpredictable because genetic variations are known to occur randomly. However, remarkable patterns of repeated convergent evolution are observed, for instance, loss of pigments by organisms living in caves. Analogous phenotypes appear in similar environments, sometimes in response to similar constraints. Alongside randomness, a certain evolutionary determinism also exists, for instance, the selection of particular phenotypes subjected to particular environmental constraints in the "evolutionary funnel." We pursue the idea that eco-evolutionary specialization is in some way determinist. The conceptual framework of phenotypic changes entailing specialization presented in this essay explains how evolution can be predicted. We also discuss how the predictability of evolution could be tested using the case of metabolic specialization through gene losses. We also put forward that microorganisms could be key models to test and possibly make headway evolutionary predictions and knowledge about evolution.

Keywords: Evolutionary Biology; Evolutionary Theories.

Graphical abstract

Figure 1

The Ecological Levels of Integration The different levels of ecological hierarchy are represented: genomic (i.e., inside the triangles), individual phenotype (i.e., a triangle) on which selection acts as engine of population dynamics (i.e., a circle), community (i.e., circle embedding populations), and ecosystems (i.e., embedding communities at a given [geographic] location). The functional level is also considered in ecology; it corresponds to the activity and roles in the ecosystem expressed by an organism or a population.

Figure 2

Phenotype Seen As a Hyper-volume in Multidimensional Space Each ridge of the volume is a trait of the phenotype. Ridges can take different values. Some of the traits may be related to others (functional trade-offs), and their variation will influence the variations in related traits. To facilitate interpretation, the volume is very homogeneous, but each side of the volume could be shaped and sized differently.

Figure 3

The “Evolutionary Funnel” Showing the Constraints That Shape Evolutionary Possibilities The first level of constraint is the intrinsic (physicochemical) properties of the genetic code that enable only restricted modification of the genome. Genome-wise, the complex network of interacting genes limits possible modifications, as any modification in a gene can have a cascade of effects on other genes. Here, the effect of pleiotropic genes is crucial as the constraints exerted on these genes are strong. The changes also have to be viable, with their core metabolic functions conserved (not carrying important modifications), whereas other accessory functions will be more readily modified (Lee and Marx, 2012). Trade-offs at phenotypic levels will also shape the possible evolutionary trajectory. Finally, the biotic and abiotic environment also constrains evolution and thus population dynamics, for example, through the available resources and the interacting species present, thereby modifying population and community dynamics. Natural selection (i.e., adaptation to the existing environment) will drive the conservation of particular adaptive solution(s).

Figure 4

Simplified Representation of the Metabolic Optimization Concept The “metabolic streamlining” hypothesis (Giovannoni, 2005; Tripp et al., 2010) is represented in a simplified way. The green rectangle represents the organism, the circles and lines schematically represent the metabolic network of the organism, and the arrows represent nutrient uptake. The yellow circles represent “activated” metabolic pathways, and the gray circles, inactivated pathways. In an environment with no constraints (left), organisms can exploit all the nutrients present (if they have the necessary capacity) and the corresponding metabolic pathways will consequently be activated. Conversely, in an environment in which the nutrient resources are constrained, say, to one-carbon source, only the metabolic pathway that is activated will be essential. The other unused pathways could, after some evolutionary time and according to streamlining hypotheses, decay (i.e., the related genes will no longer be under selection), leading to the specialization of the metabolism of the organisms. This channeled evolution trajectory is probably predictable and experimentally testable.

Figure 5

Conceptual Framework of Phenotypic Changes Leading to Specialization (A) The central hypervolume is a simplified representation of the phenotype of an organism; each ridge of the volume is a feature of the organism that can display variable values (for example, a ridge is the “color of the organism,” which can take the values beige, gray, brown, black, etc.). (A+) The expanding space of possibilities on the left (gray space of the volume) suggests that if an organism changes to a new environment with previously inexperienced parameters, it may have to develop new features, or new variations of existing features that are not part of the current phenotype (which could happen through gene duplication or gene acquisition via horizontal transfer). In this context, prediction is difficult, as one would have to identify all possible innovations and evolutionary trajectories. (A-) The reduced volume schematizes the specialization of an organism when its environment is reduced, more constrained in the range of existing parameters. In this case, predicting evolutionary trajectories and population dynamics toward a maximized local or global fitness is within the realm of possibility as we expect already existing features to be modified to optimize their activity. For example, features that enable a response to a constraint that is conserved should be enhanced, whereas features that enabled a response to constraints that were removed could decay.