Paradoxical Evolution of <i>Apis mellifera</i> Mitogenomes: Deviation From the Mutation‐Selection‐Drift Balance

Mitochondrial genome is a powerful tool for studying evolutionary biology, because it is affected by niche adaptation, energy requirements and phenotypic plasticity of organisms. Generalizations about mitogenome evolution are tricky and lead to inconsistent results. The mitogenome can contain lesser mutations than expected and escape mutational meltdown only through the balance of mutation-selection-drift. The state of equilibrium can be achieved by not being significantly affected by any evolutionary process. The reduction of variation by selective sweeps or background selection due to selection and the results of negative purifying selection by the mechanism of genetic drafting exhibit the same effect: reduction of variation on rapidly adapting genes by positive selection and rapid removal of variation from the population due to important functional limitations. Apis mellifera represents a unique model for studying mitogenome evolution, thanks to the characters about adaptation related with life style and biochemistry related with energy requirement. The evolutionary drivers of A. mellifera mitogenomes were tested using 66 mitogenome data representing 21 subspecies. First, processes of mutations/variations were evaluated in nucleotide content and its attitudes. The genome-wide mutational processes were estimated via the abundance of rearrangements and ORF remnants. Selection forces acting on mitogenomes were tested in protein-coding genes. The direction of selection was predicted using a phylogenetic tree- based inferences, and the effects of differences on the possible 3D structures of the proteins were examined. In A. mellifera mitogenomes, the mutation-selection-drift balance was biased to deviation. The balance seems to be maintained by relaxed selection phenomenon, which affects mitogenome quite indirectly. It appears to affect the total mitogenome via copies or "remnants" of the gene, without affecting the mitogenome/mitochondrial gene at the protein level, or even without major changes in the "real" nucleotide sequences of the gene. It does this by inserting repetitive sequences into the d-loop, conserved and possibly functional gene remnants (atp8) into rRNA genes, and affecting the entire genome largely through selective sweeps. Additionally, nd3 gene was positively selected in A. mellifera mitogenomes.