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The evolution of ancestral and species-specific adaptations in snowfinches at the Qinghai-Tibet Plateau.

ABSTRACT: Species in a shared environment tend to evolve similar adaptations under the influence of their phylogenetic context. Using snowfinches, a monophyletic group of passerine birds (Passeridae), we study the relative roles of ancestral and species-specific adaptations to an extreme high-elevation environment, the Qinghai-Tibet Plateau. Our ancestral trait reconstruction shows that the ancestral snowfinch occupied high elevations and had a larger body mass than most nonsnowfinches in Passeridae. Subsequently, this phenotypic adaptation diversified in the descendant species. By comparing high-quality genomes from representatives of the three phylogenetic lineages, we find that about 95% of genes under positive selection in the descendant species are different from those in the ancestor. Consistently, the biological functions enriched for these species differ from those of their ancestor to various degrees (semantic similarity values ranging from 0.27 to 0.5), suggesting that the three descendant species have evolved divergently from the initial adaptation in their common ancestor. Using a functional assay to a highly selective gene, DTL, we demonstrate that the nonsynonymous substitutions in the ancestor and descendant species have improved the repair capacity of ultraviolet-induced DNA damage. The repair kinetics of the DTL gene shows a twofold to fourfold variation across the ancestor and the descendants. Collectively, this study reveals an exceptional case of adaptive evolution to high-elevation environments, an evolutionary process with an initial adaptation in the common ancestor followed by adaptive diversification of the descendant species.

SUBMITTER: Qu Y

PROVIDER: S-EPMC8020664 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Background and aimsAccurate identification of species is essential for the majority of biological studies. However, defining species objectively and consistently remains a challenge, especially for plants distributed in remote regions where there is often a lack of sufficient previous specimens. In this study, multiple approaches and lines of evidence were used to determine species boundaries for plants occurring in the Qinghai-Tibet Plateau, using the genus Orinus (Poaceae) as a model system for an integrative approach to delimiting species.MethodsA total of 786 individuals from 102 populations of six previously recognized species were collected for niche, morphological and genetic analyses. Three plastid DNA regions (matK, rbcL and trnH-psbA) and one nuclear DNA region [internal transcribed space (ITS)] were sequenced.Key resultsWhereas six species had been previously recognized, statistical analyses based on character variation, molecular data and niche differentiation identified only two well-delimited clusters, together with a third possibly originating from relatively recent hybridization between, or historical introgression from, the other two.ConclusionsBased on a principle of integrative species delimitation to reconcile different sources of data, the results provide compelling evidence that the six previously recognized species of the genus Orinus that were examined should be reduced to two, with new circumscriptions, and a third, identified in this study, should be described as a new species. This empirical study highlights the value of applying genetic differentiation, morphometric statistics and ecological niche modelling in an integrative approach to re-circumscribing species boundaries. The results produce relatively objective, operational and unbiased taxonomic classifications of plants occurring in remote regions.

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