High-altitude adaptation is accompanied by strong signatures of purifying selection in the mitochondrial genomes of three Andean waterfowl

PLoS One. 2024 Jan 3;19(1):e0294842. doi: 10.1371/journal.pone.0294842. eCollection 2024.

Abstract

Evidence from a variety of organisms points to convergent evolution on the mitochondria associated with a physiological response to oxygen deprivation or temperature stress, including mechanisms for high-altitude adaptation. Here, we examine whether demography and/or selection explains standing mitogenome nucleotide diversity in high-altitude adapted populations of three Andean waterfowl species: yellow-billed pintail (Anas georgica), speckled teal (Anas flavirostris), and cinnamon teal (Spatula cyanoptera). We compared a total of 60 mitogenomes from each of these three duck species (n = 20 per species) across low and high altitudes and tested whether part(s) or all of the mitogenome exhibited expected signatures of purifying selection within the high-altitude populations of these species. Historical effective population sizes (Ne) were inferred to be similar between high- and low-altitude populations of each species, suggesting that selection rather than genetic drift best explains the reduced genetic variation found in mitochondrial genes of high-altitude populations compared to low-altitude populations of the same species. Specifically, we provide evidence that establishment of these three Andean waterfowl species in the high-altitude environment, coincided at least in part with a persistent pattern of negative purifying selection acting on oxidative phosphorylation (OXPHOS) function of the mitochondria. Our results further reveal that the extent of gene-specific purifying selection has been greatest in the speckled teal, the species with the longest history of high-altitude occupancy.

MeSH terms

  • Adaptation, Physiological / genetics
  • Altitude
  • Environment
  • Genetic Drift
  • Genome, Mitochondrial* / genetics
  • Mitochondria / genetics
  • Selection, Genetic

Grants and funding

We thank the many people and provincial and federal governments in Argentina, Peru, and Bolivia who assisted us with fieldwork for many years. Funding was provided by Alaska EPSCoR (NSF EPS-0092040, EPS-0346770), the National Science Foundation (DEB-0444748 and IOS-0949439), Frank M. Chapman Fund at the American Museum of Natural History, and the Kushlan Endowment for Waterbird Biology and Conservation at the University of Miami. AMG was supported by an UM College of Arts and Sciences Maytag Fellowship and Graduate Summer Research Fellowship. This work was supported in part by the high-performance computing and data storage resources operated by the Research Computing Systems Group at the University of Alaska Fairbanks, Geophysical Institute. AMG and KGM conceived the idea/design/experiment, AMG, PL and REW performed the experiments and analyzed the data, AMG, PL, REW and KGM wrote the paper. Specimen collections were carried out under University of Alaska Fairbanks IACUC protocols #02-01 and #05-05. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.