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Contributed by Donald E. Canfield, January 14, 2014 (sent for review August 26, 2013)
Significance
The relationship between the origin of animals and the oxygen content of the atmosphere is a pressing issue in historical geology. Here we challenge the widely held view that low levels of atmospheric oxygen delayed the origin of animals up until 850–542 million years ago. We provide experimental evidence suggesting that the last common ancestor of animals could have thrived in oxygen levels as low as 0.5% to 4% of present atmospheric levels, which were likely met on Earth well before animals evolved. This was achieved by observing the survival of sponges, basal animals similar to the earliest metazoans, under low-oxygen conditions in the laboratory. These results encourage us to reconsider the environmental constraints on the origin of animal life.
Abstract
A rise in the oxygen content of the atmosphere and oceans is one of the most popular explanations for the relatively late and abrupt appearance of animal life on Earth. In this scenario, Earth’s surface environment failed to meet the high oxygen requirements of animals up until the middle to late Neoproterozoic Era (850–542 million years ago), when oxygen concentrations sufficiently rose to permit the existence of animal life for the first time. Although multiple lines of geochemical evidence support an oxygenation of the Ediacaran oceans (635–542 million years ago), roughly corresponding with the first appearance of metazoans in the fossil record, the oxygen requirements of basal animals remain unclear. Here we show that modern demosponges, serving as analogs for early animals, can survive under low-oxygen conditions of 0.5–4.0% present atmospheric levels. Because the last common ancestor of metazoans likely exhibited a physiology and morphology similar to that of a modern sponge, its oxygen demands may have been met well before the enhanced oxygenation of the Ediacaran Period. Therefore, the origin of animals may not have been triggered by a contemporaneous rise in the oxygen content of the atmosphere and oceans. Instead, other ecological and developmental processes are needed to adequately explain the origin and earliest evolution of animal life on Earth.
Footnotes
↵1D.B.M. and L.M.W. contributed equally to this work.
- ↵2To whom correspondence may be addressed. E-mail: dmills{at}biology.sdu.dk or dec{at}biology.sdu.dk.
Author contributions: D.B.M., L.M.W., A.H.T., and D.E.C. designed research; D.B.M., L.M.W., C.J., B.S., and M.F. performed research; D.B.M., L.M.W., C.J., B.S., M.F., and D.E.C. analyzed data; and D.B.M., L.M.W., and D.E.C. wrote the paper.
The authors declare no conflict of interest.
See Commentary on page 3907.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1400547111/-/DCSupplemental.
Freely available online through the PNAS open access option.
Oxygen requirements of the earliest animals
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- Biological Sciences
- Evolution
- Physical Sciences
- Earth, Atmospheric, and Planetary Sciences
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