Phylogenomic analyses of the genus Drosophila reveals genomic signals of climate adaptation

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  • Rahul V. Rane
  • Victor Luria
  • Zijun Xiong
  • Jiawei Chen
  • Zimai Li
  • Renee A. Catullo
  • Philippa C. Griffin
  • Michele Schiffer
  • Stephen Pearce
  • Siu Fai Lee
  • Kerensa McElroy
  • Ann Stocker
  • Jennifer Shirriffs
  • Fiona Cockerell
  • Chris Coppin
  • Carla M. Sgrò
  • Amir Karger
  • John W. Cain
  • Jessica A. Weber
  • Gabriel Santpere
  • Marc W. Kirschner
  • Ary A. Hoffmann
  • John G. Oakeshott

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.

Original languageEnglish
JournalMolecular Ecology Resources
Volume22
Issue number4
Pages (from-to)1559-1581
Number of pages23
ISSN1755-098X
DOIs
Publication statusPublished - 2022

Bibliographical note

Publisher Copyright:
© 2021 The Authors. Molecular Ecology Resources published by John Wiley & Sons Ltd.

    Research areas

  • climate adaptation, Drosophila, incomplete lineage sorting, introgression, phylogenomics, phylostratigraphy

ID: 287072895