Boyle, Richard A; Moody, Edmund RR; Babcock, Gunnar; Mcshea, Daniel W; alvarez-Carretero, Sandra; Lenton, Timothy M; Donoghue, Philip CJ; (2025) Persistence selection between simulated biogeochemical cycle variants for their distinct effects on the Earth system. PNAS , 122 (7) , Article e2406344122. 10.1073/pnas.2406344122.

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Abstract

The average long-term impact of Darwinian evolution on Earth’s habitability remains extremely uncertain. Recent attempts to reconcile this uncertainty by “Darwinizing” nonreplicating biogeochemical processes subject to persistence-based selection conform with the historicity of the geochemical record but lack mechanistic clarity. Here, we present a theoretical framework showing how: 1) A biogeochemical “cycle-biota-variant” (CBV) can be defined non-arbitrarily as one biologically facilitated pathway for net recycling of an essential element, plus the genotypes driving the relevant interconversion reactions. 2) Distinct CBVs can be individuated if they have climatic or geochemical side effects that feed-back on relative persistence. 3) The separation of spatial/temporal scales between the dynamics of such effects and those of conventional Darwinian evolution can introduce a degree of randomness into the relationship between CBVs and their Earth system impact properties, loosely analogous to that between the biochemical causes and evolutionary effects of genetic mutation. 4) Threshold behavior in climate feedback can accentuate biotic impacts and lead to CBV-level “competitive exclusion”. 5) CBV-level persistence selection is observationally distinguishable from genotype-level selection by strong covariance between “internal” CBV properties (genotypes and reactions) and “external” climatic effects, which we argue is analogous to the covariance between fitness and traits under conventional Darwinian selection. These factors cannot circumvent the basic fact that local natural selection will often favor phenotypes that ultimately destabilize large-scale geochemical/climatic properties. However, we claim that our results nevertheless demonstrate the theoretical coherence of persistence-selection between non-replicating life–environment interaction patterns and therefore have broad biogeochemical applicability.

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