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Adaptive introgression of the beta-globin cluster in two Andean waterfowl

Abstract

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.

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Fig. 1: A simplified schematic showing how HIF-pathway-induced expression of erythropoietin (EPO) in the kidney stimulates expression of red blood cells and hemoglobin (Hb).
Fig. 2: Coalescent model illustrating how a more recently established population of yellow-billed pintails at high altitude likely acquired beneficial β-globin allele(s) from an older, more established population of speckled teal at high altitude.
Fig. 3: Function propoerties of the observed β-globin amino acid substitutions in the HbA isoform of speckled teal and yellow-billed pintail.
Fig. 4: Amino-acid polymorphisms in the adult βA and embryonic ɛ-globin genes (HBB and HBE, shown in red) are extreme outliers in genomic scans of allele-frequency differentiation between low- and high-altitude populations of speckled teal and yellow-billed pintail.
Fig. 5: Manhattan Plots showing locus-by-locus FST calculated pairwise for all SNPs for the 26 HIF-pathway genes between low- vs. high-altitude populations of speckled teal (within species comparison) and low- vs. high-altitude populations of yellow-billed pintail (within species comparison).
Fig. 6: Manhattan Plots showing locus-by-locus FST calculated pairwise for all SNPs for the α- and β-globin clusters between high-vs.-high (between species comparisons) and low-vs.-low (between-species comparisons) populations of speckled teal vs. yellow-billed pintail (bottom and top, respectively).
Fig. 7: Haplotype network for the β-globin cluster showing the 3′ coding region of capillary-sequenced HBBA), including 291 bp spanning part of intron 2 and all of exon 3 including the AlaβA116Ser and LeuβA116Met amino-acid substitutions previously characterized experimentally by Natarajan et al. (2015).
Fig. 8: Decay of linkage disequilibrium (LD) plotted for the high-altitude populations of speckled teal and yellow-billed pintail, respectively, across the β-globin cluster.

Data availability

Parsed Illumina reads are available through NCBI SRA (PRJEB11624, PRJNA508951). NCBI nucleotide accessions for the mtDNA are FJ618397-FJ618512, JN223305-JN223375, and MG520106-MG520175. NCBI nucleotide accessions for the 3′ HBB and intronic loci are FJ617703−FJ618396, GQ269874−GQ270616, and GQ272063−GQ272202. VCF files are available in Dryad (dryad.kd08516, dryad.bnzs7h4b4). Scripts associated with analysis are available on GitHub (https://github.com/amgraham07).

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Acknowledgements

We thank the many people including Pablo Tubaro and Cecilia Kopuchian and provincial and federal governments in Argentina, Bolivia, and Peru who assisted us with fieldwork for many years. This work was supported in part by the high-performance computing and data storage resources operated by both the Research Computing Systems Group (formerly Life Sicence Informatics/Arctic Regional Supercomputing) at the University of Alaska Fairbanks, Geophysical Institute, and the core facilities at Center for Genome Research and Biocomputing at Oregon State University. We thank Jay Storz, Roy Weber, Chandru Natarajan, Joana Projecto-Garcia, Angela Fago, and Hideaki Moriyama for many helpful discussions that led to a much stronger paper and for their pioneering work and insight into avian Hb function. Jay Storz and three anonymous reviewers provided helpful comments on the manuscript.

Funding

Funding was provided to KGM 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 James A. Kushlan Endowment for Waterbird Biology and Conservation from the University of Miami. AMG was supported by a University of Miami Graduate School Maytag Fellowship, and by a National Science Foundation Postdoctoral Research Fellowship in Biology (DBI-1812103).

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AMG, JLP, and KGM designed the study; VMF, AJG, and KGM provided funding; AMG, KGM, REW, and THV performed the field research and/or generated the sequence data; AMG, JLP, DAD, KW, and KGM analyzed the data and wrote the paper. All authors commented on the paper.

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Correspondence to Allie M. Graham or Kevin G. McCracken.

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Graham, A.M., Peters, J.L., Wilson, R.E. et al. Adaptive introgression of the beta-globin cluster in two Andean waterfowl. Heredity (2021). https://doi.org/10.1038/s41437-021-00437-6

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