Oxygen and animals in Earth history.

In the annals of Earth history, few associations have proven more iconic or durable than that between animals and oxygen. As early as 1919, the experimental physiologist August Krogh (1) explored the relationship between O2 and animal anatomy, and 40 y later J. R. Nursall (2) posited explicitly that metazoans appear as fossils only in uppermost Proterozoic rocks because pO2 was insufficient to support animal physiology before this time. Preston Cloud, the first great historical geobiologist, championed this idea (3), and in recent years the hypothesis has been bolstered by geochemical data that place redox transition in broad synchrony with the first animal body fossils (4). Now, however, Mills et al. (5) challenge this view of life, at least in its simplest form. The phylogenetic relationships of basal metazoans have become more clouded in recent years, but analyses least associated with apparent systematic errors place sponges as the sister group or grade to all other animals (6, 7). For this reason, as well as the clear antiquity of many poriferan lineages (8), living sponges may provide our best physiological guide to ancestral animals. Experiments by Mills et al. (5) on the temperate demosponge Halichondria panicea (Fig. 1A) indicate that these animals can live at oxygen levels as low as 0.5–4% of present-day levels (PAL), a condition likely to have characterized surface oceans long before the Ediacaran Period. Importantly, this species grows in shallow, well-oxygenated environments and apparently has no special adaptations to low oxygen. The experimental data therefore support previous theoretical suggestions that—by virtue of their basic body plan, with essentially every cell in contact with seawater (Fig. 1B)—ancestral sponges and early diploblastic animals would have had only modest oxygen requirements (9, 10). Thus, oxygen availability probably provided little impediment to the origin of animal multicellularity. The hypothesis that animals originated in a low-oxygen world gains further support from two independent sources. The first source is ecological. The full range of oxygen tensions likely to have characterized Neoproterozoic oceans can be found today, including oxygen-minimum zones (OMZs) where pO2 can be exceedingly low. Even where oxygen falls to 1–3% PAL, however, animals, mostly tiny and unmineralized, thrive (11) (because of substrate effects, sponges are often absent from the soupy sediments that characterize OMZs). Second, increasing geochemical data support the view that oxygen levels remained low—perhaps only a few percent PAL—in the mid-Neoproterozoic oceans where animals are thought to have originated (ref. 10, and references therein). Thus, as Mills et al. argue (5), explanations for animal origins must be sought elsewhere. Complex multicellular organisms in multiple clades share key features of genetics and cell biology (12), and these illuminate the mechanisms by which animals evolved complex structures. By themselves, however, these characters do not address selection pressures that may have favored simple multicellularity in Neoproterozoic oceans; these must lie elsewhere, for example, in advantages of feeding or defense against protistan predators (13). Both fossils and molecular clocks suggest that eukaryovorus protists (protists that feed by ingesting other eukaryotic cells) radiated during the Neoproterozoic Era (14). Just as carnivory is thought to have provided an ecological driver for Cambrian animal evolution, this change in the biological environment of Neoproterozoic oceans might have facilitated the evolution of multicellarity in stem group metazoans. Does this mean, then, that oxygen was irrelevant to early animal evolution? Not at all. There is a serious disconnect between molecular clock and biomarker evidence for the origin of sponges in Cryogenian oceans and their widespread appearance as fossils in Cambrian rocks (8). Mills et al.’s (5) experiments offer tantalizing evidence that although sponges may be able to tolerate very low oxygen conditions, they are sensitive to fluctuating anoxia, and that, as in bilaterian animals, smaller forms may cope better with low oxygen than larger ones. Thus, if the Fig. 1. (A) The marine demosponge Halichondria panicea investigated by Mills et al. (5); note centimeter scale in the foreground. (B) Transmission electron microscopy through the body of the calcareous sponge Sycon coactum. The ability of sponges to tolerate low oxygen is probably related to their basic body design, with only two cell layers, the external pinacoderm (p) and the internal choanoderm (c), separated by a largely inert mesohyl (m). Both cell layers are in direct contact with seawater (sw), and diffusion distances for oxygen to any cell are short. (Scale bar, 5 μm.) Thus, sponges and other small thin animals may have been able to tolerate low Proterozoic oxygen levels; however, larger, metabolically active animals, particularly carnivores, would have been excluded. Images courtesy of D. B. Mills (A) and S. Leys (B). Author contributions: A.H.K. and E.A.S. wrote the paper.