Phylogenomic analyses of the genusDrosophilareveals genomic signals of climate adaptation

Abstract

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 trends for significantly higher ratios for those in tropical and lower ratios 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.

Phylogenomics provides insights into the evolution of cactophily and host plant shifts inDrosophila

“…As shown by Oliveira et al (2012) and Suvorov et al (2021), D. hydei represents the outermost branch of the repleta group clade. However, the positions of D. hydei and D. mercatorum in our tree are at odds with recent reports showing D. mercarotum as the most basal species of the clade (Li et al, 2021;Rane et al, 2019). Relationships within the buzzatii cluster in our tree are inconsistent with previous studies (Hurtado et al, 2019;Moreyra et al, 2019), particularly for the trio D. antonietae, D. borborema, and D. koepferae, which are representatives of the main lineages defined on grounds of fixed chromosomal inversions in the serido sibling set (Ruiz et al, 2000;Hasson et al, 2019).…”

“…Within the repleta group, species that belong to the mulleri subgroup are cactophilic whereas D. hydei and D. mercatorum are dietary generalists with the ability of feeding upon rotting fruits, vegetables, and cacti. Note that the D. mercatorum genome included in our study was originally reported as D. repleta by Rane et al (2019) and assigned to the proper species by (Li et al, 2021). The genomes of D. virilis (virilis group, subgenus Drosophila), sister of the repleta group, and D. melanogaster as the only representative of the subgenus Sophophora were also included in the study (Throckmorton, 1975;Clark et al, 2007).…”

Functional divergence of the bag of marbles gene in the Drosophila melanogaster species group

“…We expanded the species sampled to include three closely related species from the yakuba complex: D. yakuba, D. santomea , and D. teissieri . We also took advantage of published population genomic data from samples of inbred lines to expand our assessment of bam variation in additional population samples for D. melanogaster (Lack et al 2015) and D. simulans and to newly assess bam variation in population samples in the montium species group ( D. serrata, D. bunnanda, D. birchii , and D. jambulina ) and the ananassae species subgroup ( D. bipectinata, D. pseudoananassae , and D. pandora ) (Li et al 2021).…”

“…We thank Daniel Matute, Brandon Cooper, Robert Unckless, Erin Kelleher, and Luciano Matzkin for the population samples they provided for this study. We thank Fang Li for working to make the variant call files from (Li et al 2021) quickly available for this study.…”

“…We used thepredicted common ancestor of D. melanogaster and D. simulans and found similar patterns of polymorphism and divergence to the smaller samples of D. melanogaster from the USA and Zimbabwe previously reported by Bauer DuMont et al (Bauer DuMont et al 2007) (Fig 5). The D. melanogaster lineage shows a strong signal of positive selection (alpha = 0.943, P=0.001) (Fig 5).For D. simulans bam, we utilized the Burnley, Victoria population sample from Li et al(Li et al 2021). We used the same common ancestral sequence as we did for the D.melanogaster analysis to calculate divergence.…”