Fig wasps are a peculiar group of insects which, for millions of years, have inhabited the enclosed syconia of fig trees. Considering the relatively closed and dark environment of fig syconia, we hypothesize that the fig wasps’ oxidative phosphorylation (OXPHOS) pathway, which is the main oxygen consumption and adenosine triphosphate (ATP) production system, may have adaptively evolved. In this study, we manually annotated the OXPHOS genes of 11 species of fig wasps, and compared the evolutionary patterns of OXPHOS genes for six pollinators and five non-pollinators. Thirteen mitochondrial protein-coding genes and 30 nuclear-coding single-copy orthologous genes were used to analyze the amino acid substitution rate and natural selection. The results showed high amino acid substitution rates of both mitochondrial and nuclear OXPHOS genes in fig wasps, implying the co-evolution of mitochondrial and nuclear genes. Our results further revealed that the OXPHOS-related genes evolved significantly faster in pollinators than in non-pollinators, and five genes had significant positive selection signals in the pollinator lineage, indicating that OXPHOS genes play an important role in the adaptation of pollinators. This study can help us understand the relationship between gene evolution and environmental adaptation.

Fig wasps are a group of insects (Hymenoptera: Chalcidoidea) that live in the compact syconia of fig trees (Moraceae: Ficus). Accurate classification and phylogenetic results are very important for studies of fig wasps, but the taxonomic statuses of some fig wasps, especially the non-pollinating subfamilies are difficult to determine, such as Epichrysomallinae and Sycophaginae. To resolve the taxonomic statuses of Epichrysomallinae and Sycophaginae, we obtained transcriptomes and mitochondrial genome (mitogenome) data for four species of fig wasps. These newly added data were combined with the data of 13 wasps (data on 11 fig wasp species were from our laboratory and two wasp species were download from NCBI). Based on the transcriptome and genome data, we obtained 145 single-copy orthologous (SCO) genes in 17 wasp species, and based on mitogenome data, we obtained 13 mitochondrial protein-coding genes (PCGs) for each of the 17 wasp species. Ultimately, we used 145 SCO genes, 13 mitochondrial PCGs and combined SCO genes and mitochondrial genes data to reconstruct the phylogenies of fig wasps using both maximum likelihood (ML) and Bayesian inference (BI) analyses. Our results suggest that both Epichrysomallinae and Sycophaginae are more closely related to Agaonidae with a high statistical support.