Overlapping attempts to falsify and Darwinize the Gaia hypothesis

Evidence for life's manifestation at the planetary scale is compelling, but arguably interpretable in terms of interactive life-environment coevolution rather than homeostatic regulation. Here, I argue that a substantive and testable Gaia hypothesis must invoke an entity that is planetary in scale, habitability-promoting, and life-specific. This necessitates a resolution to Gaia's perennial 'Darwinization problem': there is no a priori reason to expect natural selection within biological populations to favour genotypes conducive to global geochemical/climatic habitability. Three potential routes are outlined for such a resolution, differing in terms of whether the Gaia hypothesis is perceived as: (i) probably incorrect and therefore without need of Darwinization; (ii) potentially correct but associated with some life-induced habitability-promoting influence unconnected to natural selection; and (iii) potentially correct but incomplete without a natural-selection-focused description of habitability. Option (i) downplays the relevance of planetary scale properties to both terrestrial habitability and extra-terrestrial life detection, whereas (ii) sidesteps the Darwinization problem by unacceptably reducing Gaia's life-specificity, making (iii) preferable because it uniquely preserves Gaia's core properties. However, this requires that Doolittle's recent 'It's-the-song-not-the-singers' theory be supplemented with a biogeochemical/climatic description of Darwinian fitness that leads to unique predictions. I summarize preliminary attempts to derive such a description.This article is part of the discussion meeting issue 'Chance and purpose in the evolution of biospheres'.