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The Origin of Phototrophy Reveals the Importance of Priority Effects for Evolutionary Innovation

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Submitted:

25 November 2020

Posted:

27 November 2020

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Abstract
The history of life on Earth has been shaped by a series of major evolutionary innovations. While some of these innovations occur repeatedly (e.g., multicellularity), some of the most important evolutionary innovations (e.g., the origin of life itself, eukaryotes, or the genetic code) are evolutionary singularities, arising just once in the history of life. This historical fact has often been interpreted to mean that singularities are particularly difficult, low-probability evolutionary events, thus making the long-term course of life on Earth highly contingent on their chance appearances. Alternatively, singularities may arise from evolutionary priority effects, where first-movers suppress independent origins. In this paper, we disentangle these hypotheses by examining a distinctive innovation: phototrophy. The ability to use light to generate metabolic energy evolved twice, preserving information about the evolution of rare, transformative innovations that is lost in singularities. We show that the two forms of phototrophy occupy opposite ends of several key trade-offs: efficiency of light capture vs. return on investment in photosynthetic infrastructure, dependence on limiting nutrients vs. metabolic versatility, and complexity vs. simplicity. Our results suggest that phototrophy is a 'dual singularity' because phototrophic niche space is too large for the first mover to fully suppress future innovation, but not so large as to support many innovations. While often ignored over geological time scales, ecological interactions, in particular the potential for direct competition and priority effects, plays a fundamental role in the tempo and mode of major evolutionary innovations.
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Subject: Biology and Life Sciences  -   Anatomy and Physiology
Copyright: This open access article is published under a Creative Commons CC BY 4.0 license, which permit the free download, distribution, and reuse, provided that the author and preprint are cited in any reuse.
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