The relationship between evolutionary and physiological variation in hemoglobin

October 23, 2007
104 (43) 16998-17003

Abstract

Physiological and evolutionary adaptations operate at very different time scales. Nevertheless, there are reasons to believe there should be a strong relationship between the two, as together they modify the phenotype. Physiological adaptations change phenotype by altering certain microscopic parameters; evolutionary adaptation can either alter genetically these same parameters or others to achieve distinct or similar ends. Although qualitative discussions of this relationship abound, there has been very little quantitative analysis. Here, we use the hemoglobin molecule as a model system to quantify the relationship between physiological and evolutionary adaptations. We compare measurements of oxygen saturation curves of 25 mammals with those of human hemoglobin under a wide range of physiological conditions. We fit the data sets to the Monod–Wyman–Changeux model to extract microscopic parameters. Our analysis demonstrates that physiological and evolutionary change act on different parameters. The main parameter that changes in the physiology of hemoglobin is relatively constant in evolution, whereas the main parameter that changes in the evolution of hemoglobin is relatively constant in physiology. This orthogonality suggests continued selection for physiological adaptability and hints at a role for this adaptability in evolutionary change.

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Acknowledgments

We thank Walter Fontana, Frank Bunn, David Osterbur, Stuart Edelstein, Robert Winslow, John Gerhart, Bill Eaton, Stephen Stearns, Kiyohiro Imai, Takashi Yonetani, Maurizio Brunori, Tom Shimizu, Pedro Bordalo, Van Savage, and Eric Deeds for many helpful discussions. M.W.K. was supported by National Institute of Child Health Grant 5R01-HD037277-09. M.P.B. was supported by the National Science Foundation Division of Mathematical Sciences.

Supporting Information

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Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 104 | No. 43
October 23, 2007
PubMed: 17942680

Classifications

Submission history

Received: July 11, 2007
Published online: October 23, 2007
Published in issue: October 23, 2007

Keywords

  1. Baldwin effect
  2. evolvability
  3. adaptability
  4. allosteric
  5. Monod–Wyman–Changeux

Acknowledgments

We thank Walter Fontana, Frank Bunn, David Osterbur, Stuart Edelstein, Robert Winslow, John Gerhart, Bill Eaton, Stephen Stearns, Kiyohiro Imai, Takashi Yonetani, Maurizio Brunori, Tom Shimizu, Pedro Bordalo, Van Savage, and Eric Deeds for many helpful discussions. M.W.K. was supported by National Institute of Child Health Grant 5R01-HD037277-09. M.P.B. was supported by the National Science Foundation Division of Mathematical Sciences.

Notes

This article contains supporting information online at www.pnas.org/cgi/content/full/0707673104/DC1.
It was previously appreciated that L4*KT4 is an approximation to a parameter called Pm and referred to as the median oxygen pressure (21).

Authors

Affiliations

Ron Milo
Department of Systems Biology, Harvard Medical School, Boston, MA 02115; and
Jennifer H. Hou
School of Engineering and Applied Sciences, Harvard University, Cambridge, MA 02138
Michael Springer
Department of Systems Biology, Harvard Medical School, Boston, MA 02115; and
Michael P. Brenner
School of Engineering and Applied Sciences, Harvard University, Cambridge, MA 02138
Marc W. Kirschner§ [email protected]
Department of Systems Biology, Harvard Medical School, Boston, MA 02115; and

Notes

§
To whom correspondence should be addressed. E-mail: [email protected]
Contributed by Marc W. Kirschner, August 17, 2007
Author contributions: R.M., M.P.B. and M.W.K. designed research; R.M. and J.H.H. performed research; R.M., J.H.H., and M.S. analyzed data; and R.M., M.P.B., and M.W.K. wrote the paper.

Competing Interests

The authors declare no conflict of interest.

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    The relationship between evolutionary and physiological variation in hemoglobin
    Proceedings of the National Academy of Sciences
    • Vol. 104
    • No. 43
    • pp. 16721-17240

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