Abstract
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.
Highlights
The symbiotic relationship between fig trees (Moraceae, Ficus) and their pollinating fig wasps (Chalcidoidea, Agaonidae) can be traced back to 75 million years ago and represents extreme obligate mutualism [1]
We compared the amino acid substitution rates of the genes for pollinators and non-pollinators, and the results showed that the mitochondrial genes of the pollinators exhibited a higher amino acid substitution rate than those of the non-pollinators (p < 0.01); nuclear oxidative phosphorylation (OXPHOS) genes displayed the same
In the compact environment of fig syconia, where fig wasps have lived for tens of millions of years, the fig pollinators have a longer coevolutionary history with fig trees, and a longer lifetime inside syconia in their adult life history than the non-pollinators, which may indicate their different evolutionary patterns in the genes of OXPHOS pathway
Summary
The symbiotic relationship between fig trees (Moraceae, Ficus) and their pollinating fig wasps (or abbreviated as pollinators) (Chalcidoidea, Agaonidae) can be traced back to 75 million years ago and represents extreme obligate mutualism [1]. Fig trees have enclosed inflorescences (syconia), which have a narrow opening (ostiole) connecting the inside and outside world. The figs provide habitats for other wasps (Hymenoptera, Chalcidoidea), which do not pollinate figs (that is, non-pollinators). Pollinators and non-pollinators have different lifestyles related to figs, as a mature female pollinator leaves the natal fig syconium to enter a new receptive syconium for pollination and oviposition, while non-pollinators do not pollinate, and most of them only lay eggs outside syconia through the fig wall to the fig ovaries [2]. The fig pollinators and non-pollinators display different life and evolutionary histories related to the peculiar living
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