Convergent Evolution of Hemoglobin Function in High-Altitude Andean Waterfowl Involves Limited Parallelism at the Molecular Sequence Level

Authors

Chandrasekhar Natarajan, University of Nebraska-LincolnFollow
Joana Projecto-Garcia, University of Nebraska-Lincoln
Hideaki Moriyama, University of Nebraska-LincolnFollow
Roy E. Weber, Aarhus University
Violeta Muñoz-Fuentes, Estación Biológica de Doñana-CSIC, Sevilla, Spain
Andy J. Green, Estación Biológica de Doñana-CSIC, Sevilla, Spain
Cecilia Kopuchian, Centro de Ecología Aplicada del Litoral (CECOAL), Consejo Nacional de Investigaciones Cientificas y Técnicas (CONICET), Corrientes, Argentina
Pablo L. Tubaro, División Ornitología, Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’ (MACN-CONICET), Buenos Aires, Argentina
Luis Alza, University of Alaska, Fairbanks
Mariana Bulgarella, University of Alaska Fairbanks
Matthew M. Smith, University of Alaska Fairbanks
Robert E. Wilson, University of Alaska Fairbanks
Angela Fago, Aarhus University
Kevin G. McCracken, University of Alaska Fairbanks
Jay F. Storz, University of Nebraska-LincolnFollow

Date of this Version

2015

Citation

Natarajan C, Projecto-Garcia J, Moriyama H, Weber RE, Muñoz-Fuentes V, Green AJ, et al. (2015) Convergent Evolution of Hemoglobin Function in High-Altitude Andean Waterfowl Involves Limited Parallelism at the Molecular Sequence Level. PLoS Genet 11(12): e1005681

Comments

© 2015 Natarajan et al. This is an open access article distributed under the terms of the Creative Commons Attribution License

Abstract

A fundamental question in evolutionary genetics concerns the extent to which adaptive phenotypic convergence is attributable to convergent or parallel changes at the molecular sequence level. Here we report a comparative analysis of hemoglobin (Hb) function in eight phylogenetically replicated pairs of high- and low-altitude waterfowl taxa to test for convergence in the oxygenation properties of Hb, and to assess the extent to which convergence in biochemical phenotype is attributable to repeated amino acid replacements. Functional experiments on native Hb variants and protein engineering experiments based on sitedirected mutagenesis revealed the phenotypic effects of specific amino acid replacements that were responsible for convergent increases in Hb-O2 affinity in multiple high-altitude taxa. In six of the eight taxon pairs, high-altitude taxa evolved derived increases in Hb-O2 affinity that were caused by a combination of unique replacements, parallel replacements (involving identical-by-state variants with independent mutational origins in different lineages), and collateral replacements (involving shared, identical-by-descent variants derived via introgressive hybridization). In genome scans of nucleotide differentiation involving high- and low-altitude populations of three separate species, function-altering amino acid polymorphisms in the globin genes emerged as highly significant outliers, providing independent evidence for adaptive divergence in Hb function. The experimental results demonstrate that convergent changes in protein function can occur through multiple historical paths, and can involve multiple possible mutations. Most cases of convergence in Hb function did not involve parallel substitutions and most parallel substitutions did not affect Hb-O2 affinity, indicating that the repeatability of phenotypic evolution does not require parallelism at the molecular level.