It is often assumed that rising environmental oxygen concentrations played a significant role in the timing of the first appearance of animals and the trajectory of their early proliferation and diversification. The inherent large size and complexity of animals come with large energy requirements — levels of energy that can best, if not only, be acquired through aerobic respiration. There is also abundant geochemical evidence for an increase in ocean–atmosphere O2 concentrations in temporal proximity with the emergence of the group. To adequately test this hypothesis, however, a thorough understanding of the history of environmental oxygenation in the time between the first appearance of eukaryotes and the eventual appearance of animals is necessary. In this review, we summarize the evidence for the prevailing long-term conditions of the Proterozoic Eon prior to the emergence of Metazoa and go on to highlight multiple independent geochemical proxy records that suggest at least two transient oxygenation events — at ca. 1.4 and ca. 1.1 billion years ago (Ga) — during this time. These emerging datasets open the door to an important possibility: while prevailing conditions during much of this time would likely have presented challenges for early animals, there were intervals when oxygenated conditions were more widespread and could have favored yet undetermined advances in eukaryotic innovation, including critical early steps toward animal evolution.

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