Why evolvability appears to have increased over evolutionary time is an important unresolved biological question. Unlike most candidate explanations, this paper proposes that increasing evolvability can result without any pressure to adapt. The insight is that if evolvability is heritable, then an unbiased drifting process across genotypes can still create a distribution of phenotypes biased towards evolvability, because evolvable organisms diffuse more quickly through the space of possible phenotypes. Furthermore, because phenotypic divergence often correlates with founding niches, niche founders may on average be more evolvable, which through population growth provides a genotypic bias towards evolvability. Interestingly, the combination of these two mechanisms can lead to increasing evolvability without any pressure to out-compete other organisms, as demonstrated through experiments with a series of simulated models. Thus rather than from pressure to adapt, evolvability may inevitably result from any drift through genotypic space combined with evolution's passive tendency to accumulate niches.

Introduction

An unbroken hereditary chain links the simplest early replicators to the most complex modern macroscopic organisms. Observing this evolutionary trajectory raises the question of the cause for the appearance of increasing evolutionary potential, i.e. increasing evolvability [1]. Although the cause of such increase is still debated, most candidate explanations for evolvability rely on selection pressure [1]–[8], reflecting natural selection's significant explanatory power in other contexts. For example, selection on mutation or recombination rates [2], species-level selection to adapt [1], [3], selection for stability of evolved structures [3], [8], and persisting through fluctuating selective environments [5] have all been proposed as partial explanations for increasing evolvability. However, adaptive explanations may be unnecessary or at least merit more scrutiny if increasing evolvability is demonstrated without any pressure to adapt, that is, if evolvability results from a more fundamental (and potentially passive) process.

This paper investigates two such alternative hypotheses for evolvability. The first hypothesis is that if evolvability itself is heritable, then even a passive drifting process over genotypes will differentiate the evolvability of organisms, and the more evolvable of these organisms will be more likely to become phenotypically diverse and spread through niches. That is, a biased distribution of phenotypes can result from a passive drift over genotypes.

Intuitively, in a passive drift some mutations may increase an organism's evolutionary potential, while others may decrease it. Importantly, note that such passive drifting does not cause an inherent drive towards increasing evolvability when averaged over all genotypes in the entire population. However, it turns out that evolvability averaged over niches may still rise even in a purely drifting model (i.e. a model with a fixed-size population that evolves solely through genetic drift). This conclusion follows from one widely-held conception of evolvability as the capacity of an organism to “generate heritable phenotypic variation” [3], which is also the definition adopted in this paper. While evolvability is also sometimes discussed in relation to adaptation [9], [10], the chosen definition reflects a growing consensus in biology that phenotypic variability in its own right deserves study in the context of evolvability [3], [4], [6], [11]. Thus, following this definition, those organisms that are least evolvable will on average change less phenotypically from repeated mutation, while those that are more evolvable will change more, i.e. more evolvable organisms will have a higher average velocity of phenotypic change.

As a result, the phenotype space itself can act as a filter, whereby more evolvable organisms will be separated from the less evolvable over time as they radiate at different velocities throughout the phenotypic space. This sorting mechanism is similar to how a centrifuge or a western blot separates particles of different densities or charges. In other words, at any point in time the least evolvable organisms are most likely to be found clustered together within the phenotypic space, occupying niches near their evolutionary origins. In contrast, the more evolvable organisms are more likely to diverge phenotypically over time to inhabit niches divergent from their ancestors. Thus, even if the genotypic space is evolving without direction, the resulting distribution in the phenotypic space can still become biased towards the more evolvable. That is, uniformly sampling the genotype space (which is unbiased) would on average choose less evolvable organisms than would uniformly sampling the phenotype space (which is biased). The bias in the distribution of phenotypes is that less evolvable organisms are likely to be found densely concentrated in only a few niches (near their evolutionary origin), while the more evolvable organisms are more likely to spread throughout reachable niches.

Thus if a population is drifting through a genotypic space, from surveying only the phenotypic space it might be mistakenly inferred that the average evolvability over all organisms had increased, i.e. that there is a genotypic bias towards evolvability. Furthermore, the cause of this apparent increase might be misattributed to selection pressure. In reality, however, there is no selection pressure, and the average evolvability of genotypes will not have significantly changed: Only the average evolvability per niche (i.e. averaged over divergent phenotypes) will have increased. The interesting implication is that the deceptive appearance of increasing evolvability can result from a random walk over genotypes. However, the main insight is that evolvability may be self-reinforcing: A drifting process in the genotypic space may warp the phenotypic distribution in proportion to evolvability, and given a sufficiently large population, the maximum evolvability may also increase over time, which further warps the phenotypic space. Supporting this hypothesis, experiments with both an abstract mathematical model and simulated evolved machines reveal the appearance of increasing evolvability through only a drifting process.

However, while genetic drift biases only the phenotypic distribution of organisms towards greater evolvability, an additional non-adaptive mechanism may also similarly bias the genotypic distribution. This genotypic bias can result from the correlation between phenotypic divergence and establishing new niches. In other words, evolvable organisms may be more likely to lead to new ways of life [3]. Thus more evolvable organisms may become over-represented as founders of new niches, causing the resulting population growth from niche foundation to bias the genetic space also towards increasing evolvability. Thus the second hypothesis for non-adaptive evolvability increase is that founder effects in new niches tend to amplify more evolvable organisms on average. The end result is that overall evolvability, i.e. not just its appearance, may also increase over time in nature – but not due to adaptive pressure to out-compete other organisms, which is a foundational assumption that underlies many other theories for the rise of evolvability [1]–[8].

Supporting this second hypothesis, further experiments with growing populations in which evolution is initiated within a single niche, and where each niche has a limited capacity (but where selection is random within a niche) demonstrate a significant trend towards increasing genotypic evolvability over time. Importantly, the drive towards overall increasing genotypic evolvability in these experiments is qualitatively more substantial than in the drifting models alone (where the appearance of increasing evolvability results only when averaged over niches). Another abstract model and two additional models with evolved machines exhibit the same trend towards increasing genotypic evolvability without selection pressure for adaptation. The surprising conclusion is that increasing evolvability may not result from selective pressure to adapt, but may instead be an inevitable byproduct of how evolvability warps the distribution of phenotypes and the tendency for founding new niches to amplify evolvable organisms.