PRINCIPAL INVESTIGATORS: Kevin G. McCracken and Jay F. Storz
PROJECT NUMBER: IOS-0949439 and IOS-0949931
Conclusive inferences about adaptive evolution ultimately require an understanding of mechanism. Patterns of DNA sequence variation can provide suggestive evidence for a history of natural selection on a particular gene or set of genes, but these indirect inferences should serve as a stepping-off point for experiments to identify specific mechanisms of adaptation. Accordingly, the purpose of the proposed research project is to follow up a comprehensive survey of DNA sequence variation in the hemoglobin genes of Andean waterfowl to gain insight into the functional (and possibly, adaptive) significance of the observed amino acid polymorphisms. The goal of this project is to determine whether parallel amino acid substitutions in highland populations of eight species of Andean ducks have produced similar functional changes in hemoglobin-O2 affinity. This project will integrate DNA sequence data with functional experiments to identify possible mechanisms of adaptation, and will determine whether the same or different mechanisms underlie adaptation to high-altitude hypoxia in eight replicate lineages that independently colonized the high Andes. The research will provide information about the number and types of amino acid substitutions that are involved in potentially adaptive traits, and will also provide a point of contrast for studies of humans inhabiting high-altitude regions. The work will assemble a diverse team of collaborators from North America and South America, and will develop collaborations with high-altitude physiologists. A postdoc, graduate students, and undergrads, will be mentored by faculty conducting research in structural biology, biochemical physiology, and population genomics. Understanding the mechanistic basis of traits that underlie adaptation to high-altitude environments will be motivational for the conservation of Andean species, as well as their habitats. This collaborative award is co-funded by the NSF Division of Integrative Organismal Systems and by the NSF Office of International Science and Engineering, Americas Program.
When multiple species adapt independently to a shared set of environmental challenges, repeated evolutionary changes in the same trait can reveal whether natural selection typically hits on the same design solution every time, or whether it typically comes up with new, idiosyncratic solutions in different species. When repeated changes in a trait involve the same genes – or even the same mutations within those genes – then this suggests that evolution may be predisposed to follow particular pathways. For the purpose of examining repeated evolutionary changes in response to a shared selection pressure, an especially compelling natural experiment is provided by vertebrate species with lowland ancestries that have independently colonized high-altitude environments. In vertebrates, adaptation to the reduced oxygen availability at high altitude often involves changes in the biochemical function of hemoglobin, the protein in red blood cells that is responsible for transporting oxygen from the lungs to all the cells of the body. Previous research has demonstrated that high-altitude birds and mammals have often evolved hemoglobins that have an increased binding affinity for oxygen, a biochemical adaptation that enhances oxygen uptake in the blood that perfuses the lungs. The goal of our NSF-funded research project was to assess the repeatability of protein evolution by examining mechanisms of hemoglobin adaptation to hypoxia in multiple species that have independently colonized high-altitude environments. Specifically, we experimentally characterized the molecular basis of variation in hemoglobin function in multiple species of waterfowl that live at both high and low altitudes in the Peruvian Andes. We analyzed hemoglobin function in high- and low-altitude populations of 6 species (torrent ducks, crested ducks, cinnamon teals, puna teals, yellow-billed pintails, and speckled teals) as well as a pair of closely related species that are native to high- and low-altitudes (Andean duck and Orinoco goose, respectively). Our experiments revealed that high-altitude populations or species generally have evolved an increased hemoglobin-oxygen affinity relative to their lowland counterparts. There were some exceptions (e.g., the torrent ducks), which might be explained by the fact that more recent colonists of high-altitude environments have not had sufficient time to evolve fine-tuned respiratory adaptations. Among those species that independently evolved increased hemoglobin-oxygen affinities, were the changes in protein function attributable to the same mutations? To find out, we sequenced the genes that encode the different subunits of the hemoglobin protein in each of the different high- and low-altitude populations and species. We discovered that the mutations responsible for the evolved changes in hemoglobin-oxygen affinity were unique in each high-altitude population (or species, in the case of the Andean duck). These results suggest that natural selection may often achieve the same functional outcome (e.g., hemoglobin with an increased oxygen-binding affinity) in different ways in different species. The results of our research suggest that repeated evolutionary changes in protein function do not necessarily require repeated mutational changes at the molecular sequence level.
