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Predictable convergence in hemoglobin function has unpredictable molecular underpinnings

Science
21 Oct 2016
Vol 354, Issue 6310
pp. 336-339

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In convergent evolution, similar environmental conditions produce similar sets of adaptations. Does similar convergence exist in the molecular underpinnings of such morphological changes? Natarajan et al. looked across more than 50 species of birds that have adapted to different elevations to identify patterns of similarity in hemoglobin-oxygen binding affinity (see the Perspective by Bridgham). Increases in hemoglobin-oxygen binding affinity occurred in alpine species, but the molecular changes underlying the hemoglobin changes were variable. Thus, even in cases where adaptive phenotypic change is predictable, the molecular pathways to these changes may not be.
Science, this issue p. 336; see also p. 289

Abstract

To investigate the predictability of genetic adaptation, we examined the molecular basis of convergence in hemoglobin function in comparisons involving 56 avian taxa that have contrasting altitudinal range limits. Convergent increases in hemoglobin-oxygen affinity were pervasive among high-altitude taxa, but few such changes were attributable to parallel amino acid substitutions at key residues. Thus, predictable changes in biochemical phenotype do not have a predictable molecular basis. Experiments involving resurrected ancestral proteins revealed that historical substitutions have context-dependent effects, indicating that possible adaptive solutions are contingent on prior history. Mutations that produce an adaptive change in one species may represent precluded possibilities in other species because of differences in genetic background.

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Supplementary Material

Summary

Materials and Methods
Figs. S1 to S9
Tables S1 to S6
References (1733)

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Published In

Science
Volume 354 | Issue 6310
21 October 2016

Submission history

Received: 19 April 2016
Accepted: 20 July 2016
Published in print: 21 October 2016

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Acknowledgments

This work was funded by grants from the U.S. NIH (HL087216), the U.S. NSF (IOS-0949931, MCB-1517636, and MCB-1516660), and the Danish Council for Independent Research (10-084-565 and 4181-00094). We thank E. Petersen, H. Moriyama, and A. Kumar for assistance in the laboratory and C. Meiklejohn and K. Montooth for helpful suggestions. All experimental data are tabulated in the supplementary materials, and sequence data are archived in GenBank under accession numbers KX240692 to KX241466.

Authors

Affiliations

Chandrasekhar Natarajan
School of Biological Sciences, University of Nebraska, Lincoln, NE 68588, USA.
Federico G. Hoffmann
Department of Biochemistry, Molecular Biology, Entomology, and Plant Pathology and Institute for Genomics, Biocomputing, and Biotechnology, Mississippi State University, Mississippi State, MS 39762, USA.
Roy E. Weber
Zoophysiology, Department of Bioscience, Aarhus University, DK-8000 Aarhus, Denmark.
Angela Fago
Zoophysiology, Department of Bioscience, Aarhus University, DK-8000 Aarhus, Denmark.
Christopher C. Witt
Department of Biology and Museum of Southwestern Biology, University of New Mexico, Albuquerque, NM 87131, USA.
Jay F. Storz*
School of Biological Sciences, University of Nebraska, Lincoln, NE 68588, USA.

Notes

*
Corresponding author. E-mail: [email protected]

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