Gene flow in the face of countervailing selection: Adaptation to high-altitude hypoxia in the βA hemoglobin subunit of yellow-billed pintails in the Andes

Kevin G. McCracken, Mariana Bulgarella, Kevin P. Johnson, Mary K. Kuhner, Jorge Trucco, Thomas H. Valqui, Robert E. Wilson, Jeffrey L. Peters

Research output: Contribution to journalArticle

Abstract

When populations become locally adapted to contrasting environments, alleles that have high fitness in only one environment may be quickly eliminated in populations adapted to other environments, such that gene flow is partly restricted. The stronger the selection, the more rapidly immigrant alleles of lower fitness will be eliminated from the population. However, gene flow may continue to occur at unlinked loci, and adaptive divergence can proceed in the face of countervailing gene flow if selection is strong relative to migration (s > m). We studied the population genetics of the major hemoglobin genes in yellow-billed pintails (Anas georgica) experiencing contrasting partial pressures of oxygen in the Andes of South America. High gene flow and weak population subdivision were evident at seven putatively neutral loci in different chromosomal linkage groups. In contrast, amino acid replacements (Ser-β13, Ser-β116, and Met-β133) in the βA hemoglobin subunit segregated by elevation between lowland and highland populations with significantly elevated F ST. Migration rates for the βA subunit alleles were approximately 17-24 times smaller than for five unlinked reference loci, the αA hemoglobin subunit (which lacks amino acid replacements) and the mitochondrial DNA control region. The βA subunit alleles of yellow-billed pintails were half as likely to be transferred downslope, from the highlands to the lowlands, than in the opposite direction upslope. We hypothesize that migration between the lowlands and highlands is restricted by local adaptation, and the βA hemoglobin subunit is a likely target of selection related to high-altitude hypoxia; however, gene flow may be sufficiently high to retard divergence at most unlinked loci. Individuals homozygous for lowland alleles may have relatively little difficulty dispersing to the highlands initially but may experience long-term fitness reduction. Individuals homozygous for highland genotypes, in contrast, would be predicted to have difficulty dispersing to the lowlands if their hemoglobin alleles confer high oxygen affinity, predicted to result in chronic erythrocytosis at low elevation. Heterozygous individuals may have a dispersal advantage if their hemoglobin has a wider range of function due to the presence of multiple protein isoforms with a mixture of different oxygen affinities.

Original languageEnglish (US)
Pages (from-to)815-827
Number of pages13
JournalMolecular biology and evolution
Volume26
Issue number4
DOIs
StatePublished - Apr 1 2009

Keywords

  • Altiplano
  • Anas georgica
  • Anatidae
  • Ducks
  • Elevation
  • Migration
  • Oxygen binding and delivery
  • Patagonia
  • Population genetics
  • Puna
  • South America
  • Waterfowl

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics

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