Abstract A key question in evolutionary biology concerns the relative importance of different sources of adaptive genetic variation, such as de novo mutations, standing variation, and introgressive hybridization. A corollary question concerns how allelic variants derived from these different sources may influence the molecular basis of phenotypic adaptation. Here, we use a protein-engineering approach to examine the phenotypic effect of putatively adaptive hemoglobin (Hb) mutations in the high-altitude Tibetan wolf that were selectively introgressed into the Tibetan mastiff, a high-altitude dog breed that is renowned for its hypoxia tolerance. Experiments revealed that the introgressed coding variants confer an increased Hb–O2 affinity in conjunction with an enhanced Bohr effect. We also document that affinity-enhancing mutations in the β-globin gene of Tibetan wolf were originally derived via interparalog gene conversion from a tandemly linked β-globin pseudogene. Thus, affinity-enhancing mutations were introduced into the β-globin gene of Tibetan wolf via one form of intragenomic lateral transfer (ectopic gene conversion) and were subsequently introduced into the Tibetan mastiff genome via a second form of lateral transfer (introgression). Site-directed mutagenesis experiments revealed that the increased Hb–O2 affinity requires a specific two-site combination of amino acid replacements, suggesting that the molecular underpinnings of Hb adaptation in Tibetan mastiff (involving mutations that arose in a nonexpressed gene and which originally fixed in Tibetan wolf) may be qualitatively distinct from functionally similar changes in protein function that could have evolved via sequential fixation of de novo mutations during the breed’s relatively short duration of residency at high altitude.
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Introgressive Hybridization and Hypoxia Adaptation in High-Altitude Vertebrates
In natural populations of animals, a growing body of evidence suggests that introgressive hybridization may often serve as an important source of adaptive genetic variation. Population genomic studies of high-altitude vertebrates have provided strong evidence of positive selection on introgressed allelic variants, typically involving a long-term highland species as the donor and a more recently arrived colonizing species as the recipient. In high-altitude humans and canids from the Tibetan Plateau, case studies of adaptive introgression involving the HIF transcription factor, EPAS1 , have provided insights into complex histories of ancient introgression, including examples of admixture from now-extinct source populations. In Tibetan canids and Andean waterfowl, directed mutagenesis experiments involving introgressed hemoglobin variants successfully identified causative amino acid mutations and characterized their phenotypic effects, thereby providing insights into the functional properties of selectively introgressed alleles. We review case studies of adaptive introgression in high-altitude vertebrates and we highlight findings that may be of general significance for understanding mechanisms of environmental adaptation involving different sources of genetic variation.
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- Award ID(s):
- 1736249
- NSF-PAR ID:
- 10283513
- Date Published:
- Journal Name:
- Frontiers in Genetics
- Volume:
- 12
- ISSN:
- 1664-8021
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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null (Ed.)Introgression of beneficial alleles has emerged as an important avenue for genetic adaptation in both plant and animal populations. In vertebrates, adaptation to hypoxic high-altitude environments involves the coordination of multiple molecular and cellular mechanisms, including selection on the hypoxia-inducible factor (HIF) pathway and the blood-O2 transport protein hemoglobin (Hb). In two Andean duck species, a striking DNA sequence similarity reflecting identity by descent is present across the ~20 kb β-globin cluster including both embryonic (HBE) and adult (HBB) paralogs, though it was yet untested whether this is due to independent parallel evolution or adaptive introgression. In this study, we find that identical amino acid substitutions in the β-globin cluster that increase Hb-O2 affinity have likely resulted from historical interbreeding between high-altitude populations of two different distantly-related species. We examined the direction of introgression and discovered that the species with a deeper mtDNA divergence that colonized high altitude earlier in history (Anas flavirostris) transferred adaptive genetic variation to the species with a shallower divergence (A. georgica) that likely colonized high altitude more recently possibly following a range shift into a novel environment. As a consequence, the species that received these β-globin variants through hybridization might have adapted to hypoxic conditions in the high-altitude environment more quickly through acquiring beneficial alleles from the standing, hybrid-origin variation, leading to faster evolution.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fgene.2021.696484
