Evidence map›Paper›PMID 26637114›Full record

ArticlePLoS genetics2015

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

Chandrasekhar Natarajan, Joana Projecto-Garcia, Hideaki Moriyama, Roy E Weber, Violeta Muñoz-Fuentes, Andy J Green, Cecilia Kopuchian, Pablo L Tubaro, Luis Alza, Mariana Bulgarella and 5 more

Open access · goldAbstract read
In one paragraph

Article in PLoS genetics, 2015. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 69 papers.

0numbers the graph read from it
0cells of the map it votes in
69citing papers in PubMed
13.1field-weighted citation impact, top 1% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

69 citing papers in PubMed, 178 citations in OpenAlex.

  1. Article
  2. Review
  3. The genetic foundations of convergent traits.Nature reviews. Genetics · 2026
    Review
  4. Article
  5. Language models reveal a complex sequence basis for adaptive convergent evolution of protein functions.Proceedings of the National Academy of Sciences of the United States of America · 2025
    Article
  6. Article
  7. Article
  8. Gas exchange, oxygen transport and metabolism in high-altitude waterfowl.Philosophical transactions of the Royal Society of London. Series B, Biological sciences · 2025
    Review
  9. Article
  10. Article
  11. Article
  12. Article
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  17. Article
  18. Article
  19. Review
  20. Mutation bias shapes the spectrum of adaptive substitutions.Proceedings of the National Academy of Sciences of the United States of America · 2022
    Article

9 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

15 authors at 7 institutions in 5 countries.

Chandrasekhar NatarajanSchool of Biological Sciences, University of Nebraska, Lincoln, Nebraska, United States of America.
Joana Projecto-GarciaSchool of Biological Sciences, University of Nebraska, Lincoln, Nebraska, United States of America.
Hideaki MoriyamaSchool of Biological Sciences, University of Nebraska, Lincoln, Nebraska, United States of America.
Roy E WeberDepartment of Bioscience, Zoophysiology, Aarhus University, Aarhus, Denmark.
Violeta Muñoz-FuentesEstación Biológica de Doñana-CSIC, Sevilla, Spain.
Andy J GreenEstación Biológica de Doñana-CSIC, Sevilla, Spain.
Cecilia KopuchianCentro de Ecología Aplicada del Litoral (CECOAL), Consejo Nacional de Investigaciones Cientificas y Técnicas (CONICET), Corrientes, Argentina.
Pablo L TubaroDivisión Ornitología, Museo Argentino de Ciencias Naturales 'Bernardino Rivadavia' (MACN-CONICET), Buenos Aires, Argentina.
Luis AlzaInstitute of Arctic Biology and University of Alaska Museum, University of Alaska Fairbanks, Fairbanks, Alaska, United States of America.
Mariana BulgarellaInstitute of Arctic Biology and University of Alaska Museum, University of Alaska Fairbanks, Fairbanks, Alaska, United States of America.
Matthew M SmithInstitute of Arctic Biology and University of Alaska Museum, University of Alaska Fairbanks, Fairbanks, Alaska, United States of America.
Robert E WilsonInstitute of Arctic Biology and University of Alaska Museum, University of Alaska Fairbanks, Fairbanks, Alaska, United States of America.
Angela FagoDepartment of Bioscience, Zoophysiology, Aarhus University, Aarhus, Denmark.
Kevin G McCrackenInstitute of Arctic Biology and University of Alaska Museum, University of Alaska Fairbanks, Fairbanks, Alaska, United States of America.
Jay F StorzSchool of Biological Sciences, University of Nebraska, Lincoln, Nebraska, United States of America.
University of Alaska Fairbanks · USUniversity of Nebraska–Lincoln · USAarhus University · DKEstación Biológica de Doñana · ESBernardino Rivadavia Natural Sciences Museum · ARConsejo Nacional de Investigaciones Científicas y Técnicas · ARUniversity of Miami · US

Funding

Mutational Pleiotropy, Epistasis, and the Adaptive Evolution of Hemoglobin FunctionR01HL087216 · NHLBI · UNIVERSITY OF NEBRASKA LINCOLN · PI STORZ, JAY · 2008 to 2021
$4.5M
NHLBI NIH HHS HL087216NHLBI NIH HHS R01 HL087216
6 · The paper itself

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 site-directed 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.

Indexed as

Evolution, MolecularAdaptation, Physiologicalalpha-GlobinsAltitudeAnimalsbeta-GlobinsBirdsHemoglobinsOxygenPhenotypePhylogenyPolymorphism, GeneticSequence Analysis, DNAalpha-Globinsbeta-GlobinsHemoglobinsOxygen

Identifiers

PMID26637114
PMCPMC4670201
OpenAlexW2194530043

What OpenQuestion holds

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LicenceCC BY
Read underepoch 390

Registered trials

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Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.