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

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.

Ancestral predisposition toward a domesticated lifestyle in the termite-cultivated fungus Termitomyces

“…Such singularities can be interpreted as either difficult low-probability evolutionary events or, alternatively, due to evolutionary priority effects, where first-movers suppress subsequent independent origins. 15,16 The biological data we collected and our phylogenetic reconstruction allowed us to identify a set of five traits shared by Termitomyces and the non-termite-associated sister group Arthromyces: a carbohydrate-degrading profile with a reduced potential to degrade plant cell wall components, a rooting stipe (pseudorhiza), the formation of asexual spores (conidia), an insect-fecal association, and the loss of clamp connections (Figure 1). Strikingly, these traits are shared to varying degrees by other members of the termitomycetoid taxa, suggesting that termitomycetoid fungi have a predisposition to domestication.…”

Earliest Photic Zone Niches Probed by Ancestral Microbial Rhodopsins

“…Thus, the necessity of oxygen for retinal synthesis remains an open question. Despite ambiguity in the timing of rhodopsin origins relative to the GOE ( Burnetti and Ratcliff 2020 ), it seems reasonable that the expansion of oxygenated niches following the GOE aided the ecological and functional diversification of rhodopsins, both expressed in the color tuning trends we observe in our phylogenetic analysis.…”

Earliest photic zone niches probed by ancestral microbial rhodopsins

“…6). These spectral regions notably occupy the window excluded by the absorption peaks of chlorophylls and bacteriochlorophylls, potentially reflecting the evolutionary tradeoffs between retinal- and chlorophyll-/bacteriochlorophyll-based phototrophy (Burnetti and Ratcliff 2020)(Fig. 5d, Fig.…”