Photosynthesis Research

, Volume 107, Issue 1, pp 37–57

The evolutionary consequences of oxygenic photosynthesis: a body size perspective

  • Jonathan L. Payne
  • Craig R. McClain
  • Alison G. Boyer
  • James H. Brown
  • Seth Finnegan
  • Michał Kowalewski
  • Richard A. KrauseJr.
  • S. Kathleen Lyons
  • Daniel W. McShea
  • Philip M. Novack-Gottshall
  • Felisa A. Smith
  • Paula Spaeth
  • Jennifer A. Stempien
  • Steve C. Wang
Review

DOI: 10.1007/s11120-010-9593-1

Cite this article as:
Payne, J.L., McClain, C.R., Boyer, A.G. et al. Photosynth Res (2011) 107: 37. doi:10.1007/s11120-010-9593-1

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 sizeOxygenEvolutionPrecambrianMaximum sizeOptimum size

Abbreviations

PAL

Present atmospheric level (of oxygen)

Mya

Millions of years ago

Gya

Billions of years ago

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Jonathan L. Payne
    • 1
  • Craig R. McClain
    • 2
  • Alison G. Boyer
    • 3
  • James H. Brown
    • 4
  • Seth Finnegan
    • 1
    • 13
  • Michał Kowalewski
    • 5
  • Richard A. KrauseJr.
    • 6
  • S. Kathleen Lyons
    • 7
  • Daniel W. McShea
    • 8
  • Philip M. Novack-Gottshall
    • 9
  • Felisa A. Smith
    • 4
  • Paula Spaeth
    • 10
  • Jennifer A. Stempien
    • 11
  • Steve C. Wang
    • 12
  1. 1.Department of Geological and Environmental SciencesStanford UniversityStanfordUSA
  2. 2.National Evolutionary Synthesis Center (NESCent)DurhamUSA
  3. 3.Department of Ecology and Evolutionary BiologyYale UniversityNew HavenUSA
  4. 4.Department of BiologyUniversity of New MexicoAlbuquerqueUSA
  5. 5.Department of GeosciencesVirginia Polytechnic Institute and State UniversityBlacksburgUSA
  6. 6.Department of Geology and GeophysicsYale UniversityNew HavenUSA
  7. 7.Department of Paleobiology, National Museum of Natural HistorySmithsonian InstitutionWashingtonUSA
  8. 8.Department of BiologyDuke UniversityDurhamUSA
  9. 9.Department of Biological SciencesBenedictine UniversityLisleUSA
  10. 10.Natural Resources DepartmentNorthland CollegeAshlandUSA
  11. 11.Department of GeologyWashington and Lee UniversityLexingtonUSA
  12. 12.Department of Mathematics and Statistics, Swarthmore CollegeSwarthmoreUSA
  13. 13.Division of Geological and Planetary SciencesCalifornia Institute of TechnologyPasadenaUSA