Signatures of high-altitude adaptation in the major hemoglobin of five species of andean dabbling ducks

Kevin McCracken, Christopher P. Barger, Mariana Bulgarella, Kevin P. Johnson, Mary K. Kuhner, Andrew V. Moore, Jeffrey L. Peters, Jorge Trucco, Thomas H. Valqui, Kevin Winker, Robert E. Wilson

Research output: Contribution to journalArticle

32 Citations (Scopus)

Abstract

Hypoxia is one of the most, important factors affecting survival at high altitude, and the major hemoglobin protein is a likely target of selection. We compared population genetic structure in the αA and βA hemoglobin subunits (HBA2 and HBB) of five paired lowland and highland populations of Andean dabbling ducks to unlinked reference loci. In the hemoglobin genes, parallel amino acid replacements were overrepresented in highland lineages, and one to five derived substitutions occurred at external solvent-accessible positions on the α and β subunits, at α1β 1 intersubunit contacts, or in close proximity to inositolpentaphosphate (IPP) binding sites. Coalescent analyses incorporating the stochasticity of drift and mutation indicated that, hemoglobin alleles were less likely to be transferred between highland and lowland populations than unlinked alleles at five other loci. Amino acid replacements that were overrepresented in the highlands were rarely found within lowland populations, suggesting that alleles segregating at high frequency in the highlands may be maladaptive in the lowlands and vice versa. Most highland populations are probably nonmigratory and locally adapted to the Altiplano, but gene flow for several species may be sufficiently high to retard divergence at unlinked loci. Heterozygosity was elevated in the αA or βA subunits of highland populations exhibiting high gene flow between the southern lowlands and the highlands and in highland species that disperse seasonally downslope to midelevation environments from the central Andean plateau. However, elevated heterozygosity occurred more frequently in the αA subunit but not simultaneously in both subunits, suggesting that selection may be more constrained by epistasis in the βA subunit. Concordant patterns among multiple species with different evolutionary histories and depths of historical divergence and gene flow suggest, that the major hemoglobin genes of these five dabbling duck species have evolved adaptively in response to high-altitude hypoxia in the Andes.

Original languageEnglish (US)
Pages (from-to)631-650
Number of pages20
JournalAmerican Naturalist
Volume174
Issue number5
DOIs
StatePublished - Nov 2009
Externally publishedYes

Fingerprint

hemoglobin
ducks
highlands
gene flow
allele
lowlands
hypoxia
heterozygosity
amino acid
replacement
divergence
epistasis
gene
alleles
stochasticity
loci
genetic structure
population genetics
mutation
substitution

Keywords

  • Anas
  • Balancing selection
  • Hypoxia
  • Lophonetta
  • Migration
  • Waterfowl

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics

Cite this

McCracken, K., Barger, C. P., Bulgarella, M., Johnson, K. P., Kuhner, M. K., Moore, A. V., ... Wilson, R. E. (2009). Signatures of high-altitude adaptation in the major hemoglobin of five species of andean dabbling ducks. American Naturalist, 174(5), 631-650. https://doi.org/10.1086/606020

Signatures of high-altitude adaptation in the major hemoglobin of five species of andean dabbling ducks. / McCracken, Kevin; Barger, Christopher P.; Bulgarella, Mariana; Johnson, Kevin P.; Kuhner, Mary K.; Moore, Andrew V.; Peters, Jeffrey L.; Trucco, Jorge; Valqui, Thomas H.; Winker, Kevin; Wilson, Robert E.

In: American Naturalist, Vol. 174, No. 5, 11.2009, p. 631-650.

Research output: Contribution to journalArticle

McCracken, K, Barger, CP, Bulgarella, M, Johnson, KP, Kuhner, MK, Moore, AV, Peters, JL, Trucco, J, Valqui, TH, Winker, K & Wilson, RE 2009, 'Signatures of high-altitude adaptation in the major hemoglobin of five species of andean dabbling ducks', American Naturalist, vol. 174, no. 5, pp. 631-650. https://doi.org/10.1086/606020
McCracken, Kevin ; Barger, Christopher P. ; Bulgarella, Mariana ; Johnson, Kevin P. ; Kuhner, Mary K. ; Moore, Andrew V. ; Peters, Jeffrey L. ; Trucco, Jorge ; Valqui, Thomas H. ; Winker, Kevin ; Wilson, Robert E. / Signatures of high-altitude adaptation in the major hemoglobin of five species of andean dabbling ducks. In: American Naturalist. 2009 ; Vol. 174, No. 5. pp. 631-650.
@article{42be5b3df92741adb55052fef53514fa,
title = "Signatures of high-altitude adaptation in the major hemoglobin of five species of andean dabbling ducks",
abstract = "Hypoxia is one of the most, important factors affecting survival at high altitude, and the major hemoglobin protein is a likely target of selection. We compared population genetic structure in the αA and βA hemoglobin subunits (HBA2 and HBB) of five paired lowland and highland populations of Andean dabbling ducks to unlinked reference loci. In the hemoglobin genes, parallel amino acid replacements were overrepresented in highland lineages, and one to five derived substitutions occurred at external solvent-accessible positions on the α and β subunits, at α1β 1 intersubunit contacts, or in close proximity to inositolpentaphosphate (IPP) binding sites. Coalescent analyses incorporating the stochasticity of drift and mutation indicated that, hemoglobin alleles were less likely to be transferred between highland and lowland populations than unlinked alleles at five other loci. Amino acid replacements that were overrepresented in the highlands were rarely found within lowland populations, suggesting that alleles segregating at high frequency in the highlands may be maladaptive in the lowlands and vice versa. Most highland populations are probably nonmigratory and locally adapted to the Altiplano, but gene flow for several species may be sufficiently high to retard divergence at unlinked loci. Heterozygosity was elevated in the αA or βA subunits of highland populations exhibiting high gene flow between the southern lowlands and the highlands and in highland species that disperse seasonally downslope to midelevation environments from the central Andean plateau. However, elevated heterozygosity occurred more frequently in the αA subunit but not simultaneously in both subunits, suggesting that selection may be more constrained by epistasis in the βA subunit. Concordant patterns among multiple species with different evolutionary histories and depths of historical divergence and gene flow suggest, that the major hemoglobin genes of these five dabbling duck species have evolved adaptively in response to high-altitude hypoxia in the Andes.",
keywords = "Anas, Balancing selection, Hypoxia, Lophonetta, Migration, Waterfowl",
author = "Kevin McCracken and Barger, {Christopher P.} and Mariana Bulgarella and Johnson, {Kevin P.} and Kuhner, {Mary K.} and Moore, {Andrew V.} and Peters, {Jeffrey L.} and Jorge Trucco and Valqui, {Thomas H.} and Kevin Winker and Wilson, {Robert E.}",
year = "2009",
month = "11",
doi = "10.1086/606020",
language = "English (US)",
volume = "174",
pages = "631--650",
journal = "American Naturalist",
issn = "0003-0147",
publisher = "University of Chicago",
number = "5",

}

TY - JOUR

T1 - Signatures of high-altitude adaptation in the major hemoglobin of five species of andean dabbling ducks

AU - McCracken, Kevin

AU - Barger, Christopher P.

AU - Bulgarella, Mariana

AU - Johnson, Kevin P.

AU - Kuhner, Mary K.

AU - Moore, Andrew V.

AU - Peters, Jeffrey L.

AU - Trucco, Jorge

AU - Valqui, Thomas H.

AU - Winker, Kevin

AU - Wilson, Robert E.

PY - 2009/11

Y1 - 2009/11

N2 - Hypoxia is one of the most, important factors affecting survival at high altitude, and the major hemoglobin protein is a likely target of selection. We compared population genetic structure in the αA and βA hemoglobin subunits (HBA2 and HBB) of five paired lowland and highland populations of Andean dabbling ducks to unlinked reference loci. In the hemoglobin genes, parallel amino acid replacements were overrepresented in highland lineages, and one to five derived substitutions occurred at external solvent-accessible positions on the α and β subunits, at α1β 1 intersubunit contacts, or in close proximity to inositolpentaphosphate (IPP) binding sites. Coalescent analyses incorporating the stochasticity of drift and mutation indicated that, hemoglobin alleles were less likely to be transferred between highland and lowland populations than unlinked alleles at five other loci. Amino acid replacements that were overrepresented in the highlands were rarely found within lowland populations, suggesting that alleles segregating at high frequency in the highlands may be maladaptive in the lowlands and vice versa. Most highland populations are probably nonmigratory and locally adapted to the Altiplano, but gene flow for several species may be sufficiently high to retard divergence at unlinked loci. Heterozygosity was elevated in the αA or βA subunits of highland populations exhibiting high gene flow between the southern lowlands and the highlands and in highland species that disperse seasonally downslope to midelevation environments from the central Andean plateau. However, elevated heterozygosity occurred more frequently in the αA subunit but not simultaneously in both subunits, suggesting that selection may be more constrained by epistasis in the βA subunit. Concordant patterns among multiple species with different evolutionary histories and depths of historical divergence and gene flow suggest, that the major hemoglobin genes of these five dabbling duck species have evolved adaptively in response to high-altitude hypoxia in the Andes.

AB - Hypoxia is one of the most, important factors affecting survival at high altitude, and the major hemoglobin protein is a likely target of selection. We compared population genetic structure in the αA and βA hemoglobin subunits (HBA2 and HBB) of five paired lowland and highland populations of Andean dabbling ducks to unlinked reference loci. In the hemoglobin genes, parallel amino acid replacements were overrepresented in highland lineages, and one to five derived substitutions occurred at external solvent-accessible positions on the α and β subunits, at α1β 1 intersubunit contacts, or in close proximity to inositolpentaphosphate (IPP) binding sites. Coalescent analyses incorporating the stochasticity of drift and mutation indicated that, hemoglobin alleles were less likely to be transferred between highland and lowland populations than unlinked alleles at five other loci. Amino acid replacements that were overrepresented in the highlands were rarely found within lowland populations, suggesting that alleles segregating at high frequency in the highlands may be maladaptive in the lowlands and vice versa. Most highland populations are probably nonmigratory and locally adapted to the Altiplano, but gene flow for several species may be sufficiently high to retard divergence at unlinked loci. Heterozygosity was elevated in the αA or βA subunits of highland populations exhibiting high gene flow between the southern lowlands and the highlands and in highland species that disperse seasonally downslope to midelevation environments from the central Andean plateau. However, elevated heterozygosity occurred more frequently in the αA subunit but not simultaneously in both subunits, suggesting that selection may be more constrained by epistasis in the βA subunit. Concordant patterns among multiple species with different evolutionary histories and depths of historical divergence and gene flow suggest, that the major hemoglobin genes of these five dabbling duck species have evolved adaptively in response to high-altitude hypoxia in the Andes.

KW - Anas

KW - Balancing selection

KW - Hypoxia

KW - Lophonetta

KW - Migration

KW - Waterfowl

UR - http://www.scopus.com/inward/record.url?scp=70349339685&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=70349339685&partnerID=8YFLogxK

U2 - 10.1086/606020

DO - 10.1086/606020

M3 - Article

C2 - 19788356

AN - SCOPUS:70349339685

VL - 174

SP - 631

EP - 650

JO - American Naturalist

JF - American Naturalist

SN - 0003-0147

IS - 5

ER -