Mitochondria, organelles specialized for the production of Adenosine Triphosphate (ATP) and thus called the powerhouses of the cell, contain their own genome - mitogenome. Rates of mitogenomic sequence evolution are remarkably variable among bilaterian lineages, but factors underlying this variability remain poorly understood. Previous studies have identified several factors that may affect mitogenomic evolutionary rates, but their effects appear to be small and lineage-specific.  

Several studies found evidence of elevated mitogenomic evolutionary rates in isolated parasitic lineages, but the evidence is inconsistent across different studies and limited to the phylum Arthropoda. Similarly, the evidence that mitogenomic evolution is faster in species with low locomotory capacity than in those with high locomotory capacity is limited to a handful of animal lineages. Therefore, it remains unknown whether the impacts of these two phenomena are universal across the animal kingdom.  

In a new study published in Nature Communications, the research groups led by Dr. ZHANG Dong at Lanzhou University/Tibet University and Prof. WANG Guitang at the Institute of Hydrobiology (IHB) of theChinese Academy of Sciences showed that parasitic lifestyle in combination with the strength of selection for locomotory capacity explains a substantial proportion of variability in mitogenomic evolutionary rates across Bilateria.  

The researchers analyzed mitochondrial genome data of about 11,000 species of bilaterian animals classified into 25 phyla. Aside from several basal phyla, Bilateria comprise most of the phyla in the animal kingdom (≈30), so the dataset comprised ≈98% of the available animal mitogenomes in the RefSeq database of the National Center of Biotechnology Information (NCBI).    

Species were classified according to lifestyle (endoparasites, ectoparasites, parasitoids, micropredators, and free-living) and locomotory capacity (high, intermediate, and low). The researchers  found that mitogenomic evolutionary rates were distributed across the combinations of these two categorisations in the following way: endoparasites > ectoparasites with low locomotory capacity > free-living with low locomotory capacity > parasitoids > ectoparasites with high locomotory capacity > micropredators > free-living with high locomotory capacity.    

Using multilevel phylogenetic regression analysis, the researchers found that lifestyle accounted for 45% of the variation in evolutionary rates across bilaterian animals, while locomotory capacity accounted for 39%, and together they accounted for 56% of the rate variation. 

Aside from providing comprehensive answers to previously open evolutionary questions, the main novelty of the study is that it made a connection between the above two variables - lifestyle and locomotory capacity. In more detail, the researchers hypothesised that the strength of purifying selection acting on mitochondrial genomes should be positively correlated with energy expenditure, which, in turn, should be positively correlated with the strength of selection for locomotory capacity. This allowed the researchers to make and test a number of novel hypotheses, and explain certain inconsistencies in previous studies.    

Furthermore, the researchers hypothesized that free-living adults should be evolving under comparatively strong purifying selection pressure, resulting in slower overall evolutionary rates than in fully parasitic animals, and the results confirmed this. In further confirmation of their hypotheses, ectoparasites with high locomotory capacity displayed branch lengths similar to those of free-living species possessing high locomotory capacity. Moreover, the majority (approximately 90%) of extreme branch lengths within the free-living dataset were found in species with low locomotory capacity.  

Overall, the findings indicate that the major explanatory variables for mitogenomic evolution in bilaterian animals have been identified. However, since locomotory capacity did not account for all the variability across different life history categories, there are most probably other factors that are underlying the elevated evolutionary rates in parasitic lineages.   

(Editor: MA Yun)