Review

Photosynthesis Research

, Volume 107, Issue 1, pp 37-57

The evolutionary consequences of oxygenic photosynthesis: a body size perspective

  • Jonathan L. PayneAffiliated withDepartment of Geological and Environmental Sciences, Stanford University Email author 
  • , Craig R. McClainAffiliated withNational Evolutionary Synthesis Center (NESCent)
  • , Alison G. BoyerAffiliated withDepartment of Ecology and Evolutionary Biology, Yale University
  • , James H. BrownAffiliated withDepartment of Biology, University of New Mexico
  • , Seth FinneganAffiliated withDepartment of Geological and Environmental Sciences, Stanford UniversityDivision of Geological and Planetary Sciences, California Institute of Technology
  • , Michał KowalewskiAffiliated withDepartment of Geosciences, Virginia Polytechnic Institute and State University
  • , Richard A. KrauseJr.Affiliated withDepartment of Geology and Geophysics, Yale University
  • , S. Kathleen LyonsAffiliated withDepartment of Paleobiology, National Museum of Natural History, Smithsonian Institution
  • , Daniel W. McSheaAffiliated withDepartment of Biology, Duke University
    • , Philip M. Novack-GottshallAffiliated withDepartment of Biological Sciences, Benedictine University
    • , Felisa A. SmithAffiliated withDepartment of Biology, University of New Mexico
    • , Paula SpaethAffiliated withDepartment of Geological and Environmental Sciences, Stanford UniversityNatural Resources Department, Northland College
    • , Jennifer A. StempienAffiliated withDepartment of Geological and Environmental Sciences, Stanford UniversityDepartment of Geology, Washington and Lee University
    • , Steve C. WangAffiliated withDepartment of Geological and Environmental Sciences, Stanford UniversityDepartment of Mathematics and Statistics, Swarthmore College

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Abstract

The high concentration of molecular oxygen in Earth’s atmosphere is arguably the most conspicuous and geologically important signature of life. Earth’s early atmosphere lacked oxygen; accumulation began after the evolution of oxygenic photosynthesis in cyanobacteria around 3.0–2.5 billion years ago (Gya). Concentrations of oxygen have since varied, first reaching near-modern values ~600 million years ago (Mya). These fluctuations have been hypothesized to constrain many biological patterns, among them the evolution of body size. Here, we review the state of knowledge relating oxygen availability to body size. Laboratory studies increasingly illuminate the mechanisms by which organisms can adapt physiologically to the variation in oxygen availability, but the extent to which these findings can be extrapolated to evolutionary timescales remains poorly understood. Experiments confirm that animal size is limited by experimental hypoxia, but show that plant vegetative growth is enhanced due to reduced photorespiration at lower O2:CO2. Field studies of size distributions across extant higher taxa and individual species in the modern provide qualitative support for a correlation between animal and protist size and oxygen availability, but few allow prediction of maximum or mean size from oxygen concentrations in unstudied regions. There is qualitative support for a link between oxygen availability and body size from the fossil record of protists and animals, but there have been few quantitative analyses confirming or refuting this impression. As oxygen transport limits the thickness or volume-to-surface area ratio—rather than mass or volume—predictions of maximum possible size cannot be constructed simply from metabolic rate and oxygen availability. Thus, it remains difficult to confirm that the largest representatives of fossil or living taxa are limited by oxygen transport rather than other factors. Despite the challenges of integrating findings from experiments on model organisms, comparative observations across living species, and fossil specimens spanning millions to billions of years, numerous tractable avenues of research could greatly improve quantitative constraints on the role of oxygen in the macroevolutionary history of organismal size.

Keywords

Body size Oxygen Evolution Precambrian Maximum size Optimum size