Constructive Neutral Evolution: An answer for seemingly 'unnecessary' complexity

A Feb. 19 review article in the Journal of Molecular Evolution proposed that Constructive Neutral Evolution (CNE) is a useful concept in the study of evolution that should be better known among molecular and evolutionary biologists.

CNE is used to explain how a complex feature could evolve in a series of non-adaptive steps; in other words, how a biological system can become more adapted to its environment and hence more competitive without positive selection. Usually, complexity is assumed to be associated with positive selection.

A team of authors from the Biodesign Center for Mechanisms of Evolution at Arizona State University argue that making use of the "under-appreciated" CNE would enrich molecular biology and its understanding of evolutionary processes by explaining why "unnecessary" complexities can exist.

Typically, a more complex structure has more interacting parts and would be thought to have more functions or adaptive possibilities. But, biology seems to present some exceptions. Some biological features appear to have “unnecessary” complexity – the paper mentions the massive rearrangements to form the somatic ciliate genome or the seemingly “unnecessary” path of the laryngeal nerve of giraffes.

While it is somewhat speculative to call any biological feature “unnecessary” since the line between necessary and unnecessary is often a matter of discussion, at times, it is used as a hypothesis. A related scenario is when positive selection cannot account for the formation of a necessary biological feature. In both scenarios CNE is invoked to explain how biology came to possess these features.

CNE was proposed approximately 20 years ago by molecular biologists who formulated five key concepts:

(1) Excess capacities: This is a prerequisite for CNE and refers to properties "whose removal would not be harmful."

(2) Epistasis: This is the consequence of excess capacities. For genes that encode proteins with overlapping roles when one of those genes is damaged by a harmful mutation, the harmful effect of mutation may not appear due to compensation by redundancy in the organism. 

(3) Random genetic drift: This allows for the fixation of neutral mutations.

(4) Biased variation: This refers to a situation where some neutral mutational changes become more common than others, giving directionality to CNE.

(5) Purifying selection: This process "acts as a sieve" to purge harmful mutations and allow for the accumulation of non-harmful ones.

In summary, a biological system may go through the aforementioned steps resulting in increased interdependencies and complexity, but without the occurrence of any positive selection.

Other researchers, the paper reports, have characterized CNE in terms of "biological Rube Goldberg machines" that are "over-engineered to perform a single task." This is an alternative way of thinking about constructive neutral evolution.

The arrival of 'unnecessarily complex features explained by CNE

As plausible examples of complexity that may be explained by CNE, the authors list five features: gene duplication in all taxa, scrambled genes in ciliates, gRNA-mediated pan-editing in kinetoplastids, spliceosome in eukaryotes, and spliceosomal intron spread in eukaryotic genomes.

All these features involve excess capacity, suppressive epistasis, biased variation fixed via random genetic drift and interdependency.

But, the authors caution, most of these examples and others "remain speculative and await further evidence and detailed evolutionary narratives."

The paper also acknowledges the difficulty in determining adaptiveness in the complexity of a biological system in relation to a previous ancestor's features. However, they note that historical reconstructions of evolutionary history may make it "possible to improve inferences about whether a feature became more complex via adaptive or neutral processes by using modern phylogenetic and experimental methods."

The authors make a case for some complexities being unnecessary for a biological system. CNE can help explain this phenomenon, they argue.

The paper concludes: "We hope that our perspective provides some food for thought about the processes that sculpt important biological features, specifically the processes that cause them to diversity, expand, and become more complex. Our view is that by considering neutral processes like CNE, in additional to adaptive processes, richer and more accurate evolutionary narratives might be constructed for the origins of complex features."