Substantial rearrangements, single nucleotide frameshift deletion and low diversity in mitogenome of Wolbachia-infected strepsipteran endoparasitoid in comparison to its tephritid hosts

Abstract

Insect mitogenome organisation is highly conserved, yet, some insects, especially with parasitic life cycles, have rearranged mitogenomes. Furthermore, intraspecific mitochondrial diversity can be reduced by fitness-affecting bacterial endosymbionts like Wolbachia due to their maternal coinheritance with mitochondria. We have sequenced mitogenomes of the Wolbachia-infected endoparasitoid Dipterophagus daci (Strepsiptera: Halictophagidae) and four of its 22 known tephritid fruit fly host species using total genomic extracts of parasitised flies collected across > 700 km in Australia. This halictophagid mitogenome revealed extensive rearrangements relative to the four fly mitogenomes which exhibited the ancestral insect mitogenome pattern. Compared to the only four available other strepsipteran mitogenomes, the D. daci mitogenome had additional transpositions of one rRNA and two tRNA genes, and a single nucleotide frameshift deletion in nad5 requiring translational frameshifting or, alternatively, resulting in a large protein truncation. Dipterophagus daci displays an almost completely endoparasitic life cycle when compared to Strepsiptera that have maintained the ancestral state of free-living adults. Our results support the hypothesis that the transition to extreme endoparasitism evolved together with increased levels of mitogenome changes. Furthermore, intraspecific mitogenome diversity was substantially smaller in D. daci than the parasitised flies suggesting Wolbachia reduced mitochondrial diversity because of a role in D. daci fitness.

Bacterial Communities Are Less Diverse in a Strepsipteran Endoparasitoid than in Its Fruit Fly Hosts and Dominated by Wolbachia

“…Previous analyses have found that Wolbachia occurs at high prevalence in D. daci [ 28 ], and D. daci is depauperate in mitogenome diversity across large parts of its geographic distribution [ 28 , 43 ]. Because of maternal co-inheritance with mitochondria, Wolbachia may have caused a selective sweep of mitochondria due to either reproductive manipulation or beneficial host fitness effects.…”

“…Beta diversity was assessed using weighted UniFrac distance (phylogenetic relationships and relative abundance) and Bray–Curtis distance (relative abundance) to determine the microbial community variation in the four sample groups (Dd, FliesDdW, FliesDd and Flies) with pairwise comparisons (PERMANOVA) using qiime diversity beta-group-significance in QIIME 2 (v. 2019.7). Beta diversity results were also visualised using principal coordinates analysis (PCoA) plots in R. To confirm that the Wolbachia ASV of our study corresponded to the Wolbachia previously characterised from D. daci , we compared it in a multiple sequence alignment using CLUSTALW together with 16S rRNA gene sequences of w Ddac1 and w Ddac2 extracted from genome reads obtained from the Wolbachia- positive sample B. frauenfeldi 485 as part of a whole genome sequencing project [ 28 , 43 ] and with a cloned Wolbachia 16S rRNA gene (GenBank accession KC775794) sequence obtained from B. neohumeralis [ 51 ].…”

“…Therefore, due to the complete dependence of Strepsiptera on their hosts, it could be predicted that they have a less diverse microbiome. Such microbiome simplicity in parasites may be a parallel feature to the reduced morphological and genomic characteristics observed in several parasitic, ectosymbiotic and endosymbiotic organisms [ 26 , 43 – 45 ] including the reduced genomic characteristics exhibited by bacterial endosymbionts [ 46 , 47 ].…”