Abstract

Darwinian evolution operates at more restricted scales than the feedback processes within the Earth system, precluding the development of any systematic relationship between the organism-level traits favored by natural selection and the impact of these traits upon Earth’s long-term average habitability for life. “It’s-the-song-not-the-singer” theory proposes an extended understanding of natural selection to encompass differential persistence of non-replicating entities, potentially allowing for a quasi-Darwinian understanding of biogeochemical cycles. Here we use a simple stochastic model to demonstrate how persistence selection of the form invoked by “It’s-the-song-not-the-singer” can stabilize a generic nutrient recycling loop, despite its dependence upon genotypes with relatively low organism-level fitness. We present an evolutionary trajectory plausibly representative of aspects of Precambrian biogeochemical cycles, involving persistence-based selection for recycling via fluctuations in abiotic boundary conditions and strong genetic drift. We illustrate how self-perpetuating life-environment correlation patterns, as opposed to specific state-values, may help empirically distinguish “It’s-the-song-not-the-singer” from conventional Earth-system feedbacks.

Highlights

  • Darwinian evolution operates at more restricted scales than the feedback processes within the Earth system, precluding the development of any systematic relationship between the organism-level traits favored by natural selection and the impact of these traits upon Earth’s long-term average habitability for life

  • Lovelock’s “Gaia” hypothesis suggested that a planetary-scale homeostatic system emerges from life’s interaction with the abiotic environment, which tends to maintain Earth’s average long-term habitability for life[1]. This idea stimulated a longrunning debate concerning whether there is any legitimate sense in which life keeps the Earth in a state that is good for life, and how the biota’s global-scale impact relates to the local, futureinsensitive scope of natural selection[2–4]

  • The Earth system is characterized by global-scale biologically driven recycling of essential elements, such that the flux into photo-synthesizers of several essential elements greatly exceeds their influx into the biosphere from abiotic sources[17]

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Summary

Introduction

Darwinian evolution operates at more restricted scales than the feedback processes within the Earth system, precluding the development of any systematic relationship between the organism-level traits favored by natural selection and the impact of these traits upon Earth’s long-term average habitability for life. Lovelock’s “Gaia” hypothesis suggested that a planetary-scale homeostatic system emerges from life’s interaction with the abiotic environment, which tends to maintain Earth’s average long-term habitability for life[1] This idea stimulated a longrunning debate concerning whether there is any legitimate sense in which life keeps the Earth in a state that is good for life, and how the biota’s global-scale impact relates to the local, futureinsensitive scope of natural selection[2–4]. The Earth system is characterized by global-scale biologically driven recycling of essential elements, such that the flux into photo-synthesizers of several essential elements greatly exceeds their influx into the biosphere from abiotic sources[17] (for carbon by a factor of ~200, for nitrogen ~500–1300, for phosphorus >100018, and for sulfur ~108,19) Evidence of this sort begs the question of precisely how and why the by-products of life appear to be more conducive to the persistence of habitability than by-products of abiotic processes on lifeless planets. Despite years of polarized debate, no consensus has emerged as to what (if anything) life’s putative habitability promoting influence is supposed to be, or how any such influence relates to natural selection 20

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