Preprint Article Version 1 Preserved in Portico This version is not peer-reviewed

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

Version 1 : Received: 25 November 2020 / Approved: 27 November 2020 / Online: 27 November 2020 (16:52:24 CET)
Version 2 : Received: 30 November 2020 / Approved: 1 December 2020 / Online: 1 December 2020 (09:44:13 CET)
Version 3 : Received: 18 December 2020 / Approved: 21 December 2020 / Online: 21 December 2020 (11:29:19 CET)

How to cite: Burnetti, A.; Ratcliff, W. The Origin of Phototrophy Reveals the Importance of Priority Effects for Evolutionary Innovation. Preprints 2020, 2020110700 (doi: 10.20944/preprints202011.0700.v1). Burnetti, A.; Ratcliff, W. The Origin of Phototrophy Reveals the Importance of Priority Effects for Evolutionary Innovation. Preprints 2020, 2020110700 (doi: 10.20944/preprints202011.0700.v1).

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.

Subject Areas

photosynthesis; phototrophy; priority effects

Comments (1)

Comment 1
Received: 2 December 2020
Commenter: Denis Murphy
The commenter has declared there is no conflict of interests.
Comment: I found this a really stimulating and interesting read. A few minor comments: Nobody uses the terms archaebacteria or eubacteria now - there are only two major Divisions of Life, archaea and bacteria. Eukaryotes branch deeply inside the Asgard clade of archaea. You do not really discuss the controversy about what came first in evolution, oxygenic or non oxygenic PHS. People like Tanai Cardona have provided some compelling evidence that oxygenic PHS was first and the other forms are derived from it. This might be an interesting topic to consider in your thesis.
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