Abstract

Evolution works by adaptation and exaptation. At an organismal level, exaptation and adaptation are seen in the formation of organelles and the advent of multicellularity. At the sub-organismal level, molecular systems such as proteins and RNAs readily undergo adaptation and exaptation. Here we suggest that the concepts of adaptation and exaptation are universal, synergistic, and recursive and apply to small molecules such as metabolites, cofactors, and the building blocks of extant polymers. For example, adenosine has been extensively adapted and exapted throughout biological evolution. Chemical variants of adenosine that are products of adaptation include 2′ deoxyadenosine in DNA and a wide array of modified forms in mRNAs, tRNAs, rRNAs, and viral RNAs. Adenosine and its variants have been extensively exapted for various functions, including informational polymers (RNA, DNA), energy storage (ATP), metabolism (e.g., coenzyme A), and signaling (cyclic AMP). According to Gould, Vrba, and Darwin, exaptation imposes a general constraint on interpretation of history and origins; because of exaptation, extant function should not be used to explain evolutionary history. While this notion is accepted in evolutionary biology, it can also guide the study of the chemical origins of life. We propose that (i) evolutionary theory is broadly applicable from the dawn of life to the present time from molecules to organisms, (ii) exaptation and adaptation were important and simultaneous processes, and (iii) robust origin of life models can be constructed without conflating extant utility with historical basis of origins.

Highlights

  • Evolution is a dogged tinkerer (Jacob 1977), sculpting by adaptation and purloining by exaptation

  • While the term exaptation was coined by Gould and Vrba in the early 1980s (Gould and Vrba 1982; Gould 2002), the concept was familiar to Darwin, who recognized that the swim bladder in fish was originally used for flotation, and was thereafter co-opted for a very different purpose: respiration (Darwin 1859)

  • We suggest that exaptive/adaptive recursion was as important during prebiotic chemical evolution and early biology as it is in extant biology, and that RNA was not exempt

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Summary

Introduction

Evolution is a dogged tinkerer (Jacob 1977), sculpting by adaptation and purloining by exaptation. Keywords Exaptation · Evolution · Recursion · Chemical origins of life · Metabolites We suggest that in biology, exaptive and adaptive processes (i) are coupled and synergistic; these processes can radically accelerate each other, (ii) are prevalent on broad biological scales, from small molecules to organisms, (iii) have operated over deep time, from chemical evolution during the origins of life, to contemporary biology, and (iv) are recursive, endlessly creating, and relaunching from new landscapes.

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