Modeling Variable Phanerozoic Oxygen Effects on Physiology and Evolution
Geochemical approximation of Earth’s atmospheric O2 level over geologic time prompts hypotheses linking hyper- and hypoxic atmospheres to transformative events in the evolutionary history of the biosphere. Such correlations, however, remain problematic due to the relative imprecision of the timing and scope of oxygen change and the looseness of its overlay on the chronology of key biotic events such as radiations, evolutionary innovation, and extinctions. There are nevertheless general attributions of atmospheric oxygen concentration to key evolutionary changes among groups having a primary dependence upon oxygen diffusion for respiration. These include the occurrence of Devonian hypoxia and the accentuation of air-breathing dependence leading to the origin of vertebrate terrestriality, the occurrence of Carboniferous-Permian hyperoxia and the major radiation of early tetrapods and the origins of insect flight and gigantism, and the Mid-Late Permian oxygen decline accompanying the Permian extinction. However, because of variability between and error within different atmospheric models, there is little basis for postulating correlations outside the Late Paleozoic. Other problems arising in the correlation of paleo-oxygen with significant biological events include tendencies to ignore the role of blood pigment affinity modulation in maintaining homeostasis, the slow rates of O2 change that would have allowed for adaptation, and significant respiratory and circulatory modifications that can and do occur without changes in atmospheric oxygen. The purpose of this paper is thus to refocus thinking about basic questions central to the biological and physiological implications of O2 change over geological time.
KeywordsHypoxia Hyperoxia Evolution Tetrapod Paleozoic Paleoatmosphere Oxygen
The authors thank W. Milsom, J. Harrison, and R. Roach for their comments on this manuscript and their help with its presentation at the 2011 International Hypoxia Symposium. N.C. Wegner and C.J. Jew were supported by NSF grants IOS-0922569 and IOS-0817774 during the writing of this paper.
- 8.Carroll RL. Vertebrate paleontology and evolution. New York, NY: WH Freeman and Company; 1988. p. 698.Google Scholar
- 10.Clack JA. Gaining ground: the origin and evolution of tetrapods. Bloomington, IN: Indiana University Press; 2002. p. 369.Google Scholar
- 14.Dahl TW, Hammarlund EU, Anbar AD, Bond DPG, Gill BC, Gordon GW, Knoll AH, Nielsen AT, Schovsbo NH, Canfield DE. Devonian rise in atmospheric oxygen correlated to the radiations of terrestrial plants and large predatory fish. Proc Natl Acad Sci U S A. 2010;107:17911–5.CrossRefPubMedPubMedCentralGoogle Scholar
- 17.Erwin DH. The great Paleozoic crisis: life and death in the Permian. New York, NY: Columbia University Press; 1993. p. 327.Google Scholar
- 20.Feder ME. Integrating the ecology and physiology of plethodontid salamanders. Herpetologica. 1983;39:291–310.Google Scholar
- 27.Graham JB. Air-breathing fishes: evolution, diversity, and adaptation. San Diego, CA: Academic; 1997. p. 299.Google Scholar
- 50.Shubin N. Your inner fish: a journey into the 35-billion-year history of the human body. New York, NY: Random House; 2008. p. 229.Google Scholar
- 57.Ward PD. Out of thin air: dinosaurs, birds, and Earth’s early atmosphere. Washington, DC: John Henry Press; 2006. p. 282.Google Scholar