Phylogenomic analyses of the genus Drosophila reveals genomic signals of climate adaptation
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Phylogenomic analyses of the genus Drosophila reveals genomic signals of climate adaptation. / Li, Fang; Rane, Rahul V.; Luria, Victor; Xiong, Zijun; Chen, Jiawei; Li, Zimai; Catullo, Renee A.; Griffin, Philippa C.; Schiffer, Michele; Pearce, Stephen; Lee, Siu Fai; McElroy, Kerensa; Stocker, Ann; Shirriffs, Jennifer; Cockerell, Fiona; Coppin, Chris; Sgrò, Carla M.; Karger, Amir; Cain, John W.; Weber, Jessica A.; Santpere, Gabriel; Kirschner, Marc W.; Hoffmann, Ary A.; Oakeshott, John G.; Zhang, Guojie.
In: Molecular Ecology Resources, Vol. 22, No. 4, 2022, p. 1559-1581.Research output: Contribution to journal › Journal article › Research › peer-review
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TY - JOUR
T1 - Phylogenomic analyses of the genus Drosophila reveals genomic signals of climate adaptation
AU - Li, Fang
AU - Rane, Rahul V.
AU - Luria, Victor
AU - Xiong, Zijun
AU - Chen, Jiawei
AU - Li, Zimai
AU - Catullo, Renee A.
AU - Griffin, Philippa C.
AU - Schiffer, Michele
AU - Pearce, Stephen
AU - Lee, Siu Fai
AU - McElroy, Kerensa
AU - Stocker, Ann
AU - Shirriffs, Jennifer
AU - Cockerell, Fiona
AU - Coppin, Chris
AU - Sgrò, Carla M.
AU - Karger, Amir
AU - Cain, John W.
AU - Weber, Jessica A.
AU - Santpere, Gabriel
AU - Kirschner, Marc W.
AU - Hoffmann, Ary A.
AU - Oakeshott, John G.
AU - Zhang, Guojie
N1 - Publisher Copyright: © 2021 The Authors. Molecular Ecology Resources published by John Wiley & Sons Ltd.
PY - 2022
Y1 - 2022
N2 - Many Drosophila species differ widely in their distributions and climate niches, making them excellent subjects for evolutionary genomic studies. Here, we have developed a database of high-quality assemblies for 46 Drosophila species and one closely related Zaprionus. Fifteen of the genomes were newly sequenced, and 20 were improved with additional sequencing. New or improved annotations were generated for all 47 species, assisted by new transcriptomes for 19. Phylogenomic analyses of these data resolved several previously ambiguous relationships, especially in the melanogaster species group. However, it also revealed significant phylogenetic incongruence among genes, mainly in the form of incomplete lineage sorting in the subgenus Sophophora but also including asymmetric introgression in the subgenus Drosophila. Using the phylogeny as a framework and taking into account these incongruences, we then screened the data for genome-wide signals of adaptation to different climatic niches. First, phylostratigraphy revealed relatively high rates of recent novel gene gain in three temperate pseudoobscura and five desert-adapted cactophilic mulleri subgroup species. Second, we found differing ratios of nonsynonymous to synonymous substitutions in several hundred orthologues between climate generalists and specialists, with significant higher trends for those in tropical and lower trends for those in temperate-continental specialists respectively than those in the climate generalists. Finally, resequencing natural populations of 13 species revealed tropics-restricted species generally had smaller population sizes, lower genome diversity and more deleterious mutations than the more widespread species. We conclude that adaptation to different climates in the genus Drosophila has been associated with large-scale and multifaceted genomic changes.
AB - Many Drosophila species differ widely in their distributions and climate niches, making them excellent subjects for evolutionary genomic studies. Here, we have developed a database of high-quality assemblies for 46 Drosophila species and one closely related Zaprionus. Fifteen of the genomes were newly sequenced, and 20 were improved with additional sequencing. New or improved annotations were generated for all 47 species, assisted by new transcriptomes for 19. Phylogenomic analyses of these data resolved several previously ambiguous relationships, especially in the melanogaster species group. However, it also revealed significant phylogenetic incongruence among genes, mainly in the form of incomplete lineage sorting in the subgenus Sophophora but also including asymmetric introgression in the subgenus Drosophila. Using the phylogeny as a framework and taking into account these incongruences, we then screened the data for genome-wide signals of adaptation to different climatic niches. First, phylostratigraphy revealed relatively high rates of recent novel gene gain in three temperate pseudoobscura and five desert-adapted cactophilic mulleri subgroup species. Second, we found differing ratios of nonsynonymous to synonymous substitutions in several hundred orthologues between climate generalists and specialists, with significant higher trends for those in tropical and lower trends for those in temperate-continental specialists respectively than those in the climate generalists. Finally, resequencing natural populations of 13 species revealed tropics-restricted species generally had smaller population sizes, lower genome diversity and more deleterious mutations than the more widespread species. We conclude that adaptation to different climates in the genus Drosophila has been associated with large-scale and multifaceted genomic changes.
KW - climate adaptation
KW - Drosophila
KW - incomplete lineage sorting
KW - introgression
KW - phylogenomics
KW - phylostratigraphy
U2 - 10.1111/1755-0998.13561
DO - 10.1111/1755-0998.13561
M3 - Journal article
C2 - 34839580
AN - SCOPUS:85120711926
VL - 22
SP - 1559
EP - 1581
JO - Molecular Ecology
JF - Molecular Ecology
SN - 0962-1083
IS - 4
ER -
ID: 287072895