Multiple independent origins of neoteny reveal convergent relaxation of mitochondrial selection in beetles

Mitochondrial genome evolution is shaped by organismal energy demands, with high-performance lineages typically showing stronger purifying selection on oxidative phosphorylation (OXPHOS) genes. We tested this relationship in Elateriformia beetles by analyzing 132 mitochondrial genomes from 15 families, categorizing species as heavily sclerotized active flyers (HARD), weakly sclerotized with reduced flight (WEAK), or sedentary larviform neotenic forms (NEOTENIC). PAML branch models revealed that dN/dS ratios varied systematically across all 13 protein-coding genes, with HARD lineages showing the strongest purifying selection, WEAK intermediate, and NEOTENIC the weakest, a pattern most pronounced in ATP8, which showed > 22-fold variation between categories. RELAX analyses confirmed that elevated dN/dS in neotenic lineages reflects weakened purifying selection rather than positive selection. Neotenic lineages also showed reduced GC content consistent with relaxed constraints. These patterns were consistent across multiple independent neotenic origins separated by > 200 million years, demonstrating that developmental shifts reallocating energy from locomotion to reproduction predictably relax mitochondrial OXPHOS constraints. Our findings extend metabolic rate principles established in vertebrates to hyper-diverse terrestrial arthropods.