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1. Introgressive Hybridization and Hypoxia Adaptation in High-Altitude Vertebrates

   https://doi.org/10.3389/fgene.2021.696484  

   Storz, Jay F.; Signore, Anthony V. (June 2021, Frontiers in Genetics)

   null (Ed.)

   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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2. Ancient hybridization leads to the repeated evolution of red flowers across a monkeyflower radiation

   https://doi.org/10.1093/evlett/qrad024  

   Short, Aidan W.; Streisfeld, Matthew A. (June 2023, Evolution Letters)

   Abstract The reuse of old genetic variation can promote rapid diversification in evolutionary radiations, but in most cases, the historical events underlying this divergence are not known. For example, ancient hybridization can generate new combinations of alleles that sort into descendant lineages, potentially providing the raw material to initiate divergence. In the Mimulus aurantiacus species complex, there is evidence for widespread gene flow among members of this radiation. In addition, allelic variation in the MaMyb2 gene is responsible for differences in flower color between the closely related ecotypes of subspecies puniceus, contributing to reproductive isolation by pollinators. Previous work suggested that MaMyb2 was introgressed into the red-flowered ecotype of puniceus. However, additional taxa within the radiation have independently evolved red flowers from their yellow-flowered ancestors, raising the possibility that this introgression had a more ancient origin. In this study, we used repeated tests of admixture from whole-genome sequence data across this diverse radiation to demonstrate that there has been both ancient and recurrent hybridization in this group. However, most of the signal of this ancient introgression has been removed due to selection, suggesting that widespread barriers to gene flow are in place between taxa. Yet, a roughly 30 kb region that contains the MaMyb2 gene is currently shared only among the red-flowered taxa. Patterns of admixture, sequence divergence, and extended haplotype homozygosity across this region confirm a history of ancient hybridization, where functional variants have been preserved due to positive selection in red-flowered taxa but lost in their yellow-flowered counterparts. The results of this study reveal that selection against gene flow can reduce genomic signatures of ancient hybridization, but that historical introgression can provide essential genetic variation that facilitates the repeated evolution of phenotypic traits between lineages. 

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3. Ecological Diversification in an Adaptive Radiation of Plants: The Role of De Novo Mutation and Introgression

   https://doi.org/10.1093/molbev/msae007  

   Stone, Benjamin W; Wessinger, Carolyn A (January 2024, Molecular Biology and Evolution)

   Josephs, Emily (Ed.)

   Abstract Adaptive radiations are characterized by rapid ecological diversification and speciation events, leading to fuzzy species boundaries between ecologically differentiated species. Adaptive radiations are therefore key systems for understanding how species are formed and maintained, including the role of de novo mutations versus preexisting variation in ecological adaptation and the genome-wide consequences of hybridization events. For example, adaptive introgression, where beneficial alleles are transferred between lineages through hybridization, may fuel diversification in adaptive radiations and facilitate adaptation to new environments. In this study, we employed whole-genome resequencing data to investigate the evolutionary origin of hummingbird-pollinated flowers and to characterize genome-wide patterns of phylogenetic discordance and introgression in Penstemon subgenus Dasanthera, a small and diverse adaptive radiation of plants. We found that magenta hummingbird-adapted flowers have apparently evolved twice from ancestral blue-violet bee-pollinated flowers within this radiation. These shifts in flower color are accompanied by a variety of inactivating mutations to a key anthocyanin pathway enzyme, suggesting that independent de novo loss-of-function mutations underlie the parallel evolution of this trait. Although patterns of introgression and phylogenetic discordance were heterogenous across the genome, a strong effect of gene density suggests that, in general, natural selection opposes introgression and maintains genetic differentiation in gene-rich genomic regions. Our results highlight the importance of both de novo mutation and introgression as sources of evolutionary change and indicate a role for de novo mutation in driving parallel evolution in adaptive radiations. 

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4. A shared genetic basis of mimicry across swallowtail butterflies points to ancestral co-option of doublesex

   https://doi.org/10.1038/s41467-019-13859-y  

   Palmer, Daniela H.; Kronforst, Marcus R. (January 2020, Nature Communications)

   Abstract Uncovering whether convergent adaptations share a genetic basis is consequential for understanding the evolution of phenotypic diversity. This information can help us understand the extent to which shared ancestry or independent evolution shape adaptive phenotypes. In this study, we first ask whether the same genes underlie polymorphic mimicry inPapilioswallowtail butterflies. By comparing signatures of genetic variation between polymorphic and monomorphic species, we then investigate how ancestral variation, hybridization, and independent evolution contributed to wing pattern diversity in this group. We report that a single gene,doublesex (dsx), controls mimicry across multiple taxa, but with species-specific patterns of genetic differentiation and linkage disequilibrium. In contrast to widespread examples of phenotypic evolution driven by introgression, our analyses reveal distinct mimicry alleles. We conclude that mimicry evolution in this group was likely facilitated by ancestral polymorphism resulting from early co-option ofdsxas a mimicry locus, and that evolutionary turnover ofdsxalleles may underlie the wing pattern diversity of extant polymorphic and monomorphic lineages. 

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

   https://doi.org/https://doi.org/10.1038/s41437-021-00437-6  

   Graham, Allie M; Peters, Jeffrey L; Wilson, Robert E; Muñoz-Fuentes, Violeta; Green, Andy J; Dorfsman, Daniel A; Valqui, Thomas H; Winker, Kevin; McCracken, Kevin G (April 2021, Heredity)

   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. 

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