Comparative Evidence of an Exceptional Impact of Gene Duplication on the Developmental Evolution of Drosophila and the Higher Diptera

Abstract

The importance of gene duplication in developmental body plan evolution is wellestablished, but for many megadiverse clades such as true flies (Diptera), a comprehensive understanding is still just emerging through comparative genomics. In a survey of 377 developmental gene families, we found that in addition to the pea aphid, which has been previously shown to be genome-wide enriched with gene duplicates and was included as positive control, more than twice as many expanded developmental gene families were observed in Drosophila (49) compared to mosquito (21), flour beetle (20), and honeybee (14). Synonymous sequence divergence estimates and ortholog conservation analyses in additional dipteran genomes revealed that most Drosophila gene duplicates are ancient and accumulated during a time window that reaches back to the origin of brachyceran flies, ∼180 million years ago. Further, available genetic data suggest that more than half of the Drosophila developmental gene duplicates remained partially or even fully redundant despite their ancient separation. We therefore speculate that the exceptional accumulation of developmental gene duplicates in Drosophila and the higher Diptera was proximally driven by the evolution of fast development, benefiting from increased genetic robustness. At the same time, the concomitant increase of opportunities for gene duplicate diversification appears to have been a source for developmental and phenotypic innovation during the unparalleled diversification of brachyceran Diptera.

Genomic signatures of globally enhanced gene duplicate accumulation in the megadiverse higher Diptera fueling intralocus sexual conflict resolution

“…Lineage-specific gene family expansions were inferred via a previously described bioinformatic pipeline involving sequence similarity threshold filtering, reciprocal BLAST tests, and, in a subset of cases, gene tree reconstruction (Bao et al, 2018). Running a comparison to our previously manually curated sample of 377 developmental gene families for validation analysis (Drăghici, 2011;Bao et al, 2018), we obtained evidence of 90% or better accuracy (percentage of true positives) and 85% or better specificity (percentage of true negatives) for our automated gene family analysis pipeline (Supplemental Data File 2).…”

“…Studying the evolutionary histories of vision-related genes in insect genome models, we previously noted an unusually high number of duplicated genes in Drosophila melanogaster (Bao & Friedrich, 2009). In a followup study of over 350 developmental gene families, we discovered a preponderance of ancient, yet lineage-specific gene duplicates in Drosophila and the higher Diptera (Brachycera) (Bao et al, 2018). Moreover, more than 50% of these lineage-specific developmental gene duplications retained partial or complete genetic redundancy despite their ancient separation.…”

“…Gene duplication and classification were conducted by adopting the pipeline developed in our previous analysis of developmental gene duplicates (Bao et al, 2018). In short, species-specific protein databases (RefSeq and OGS when available) were downloaded from GenBank or respective genome project websites.…”

“…In order to compare the validation data from our previous analysis of a manually curated subset of 377 validation gene families (Drăghici, 2011;Bao et al, 2018) with the genome-wide duplication identification output (Supplemental Data File 2), every individual gene in the two data sets was assigned with a with a six-digit code, which reflected its inferred gene duplication history. Genes with 1:1 orthologs in all four lineages were assigned with the code 100000.…”

“…This led us to hypothesize that the exceptional accumulation of developmental gene duplicates in Drosophila and the higher Diptera was of adaptive nature by increasing genetic robustness as a requirement for the fast development of brachyceran Diptera such as Drosophila. At the same time, the similarly higher number of structural vision genes gave reason to suspect the possibility of a genome-wide increase of gene duplicate accumulation in the higher Diptera (Bao & Friedrich, 2009;Bao et al, 2018).…”