Transition–Transversion Bias at the CYTB Gene Level in the Order Cypriniformes (Actinopterygii) as Evidence for the Influence of Metabolic Rate on Molecular Evolutionary Rate

ABSTRACT

A positive relationship between metabolic rate and the rate of mutation accumulation is regarded as a core prediction of the metabolic theory of ecology; however, empirical support for this relationship remains limited. One indirect but rigorous approach to testing this hypothesis is to analyze the transition–transversion bias across increasing levels of genetic divergence. This approach allows comparison of evolutionary substitution patterns among taxonomic groups that differ in metabolic rate, which can be inferred from body size and species‐specific body temperature. Because transitions largely arise from spontaneous molecular processes while transversions are more strongly associated with oxidative DNA damage. These two mutation types exhibit distinct origins and mutational spectra, comparison of which will allow us to estimate the rate of mutation caused by oxidative DNA damage in taxonomic groups with different metabolic rates. The order Cypriniformes represents an excellent model system for such analyses because it includes both small‐ and large‐bodied lineages distributed across tropical and temperate climatic zones. To identify patterns of evolutionary transition–transversion bias in the mitochondrial CYTB gene among cypriniform families and subfamilies differing in climatic affiliation and body size Families and subfamilies inhabiting temperate regions exhibit increasing transition frequencies and decreasing transversion frequencies with increasing genetic divergence, resulting in a pronounced transition–transversion bias. In contrast, tropical taxa showed elevated transversion frequencies and a substantially weaker bias. Taxa distributed across both climatic zones displayed intermediate characteristics. Large‐bodied fishes exhibited higher transition frequencies and lower transversion frequencies than small‐bodied taxa, resulting in a stronger transition–transversion bias. The greatest contrast was observed between small‐bodied tropical taxa and large‐bodied temperate taxa. The accelerated accumulation of transversions relative to transitions in taxa with higher metabolic intensity—small‐bodied fishes and tropical lineages—provides direct evidence for a positive relationship between metabolic rate and the rate of mutational processes, as well as a negative association between body size and mutation rate. Elevated transversion frequencies in tropical cypriniforms additionally support the evolutionary rate hypothesis, according to which warm and climatically stable environments promote accelerated molecular evolution.