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Mitonuclear Discordance of Beetles Shaped by Incomplete Lineage Sorting and Introgression Under Loose Interaction Mechanism

Tianyou Zhao,Pingzhou Zhu,Q. Liu,Ling Ma,Ye Xu,Liang Lü,Y. Duan,Fan Song,Li Tian,Wanzhi Cai,Hu Li

Published 2025 in Molecular biology and evolution

ABSTRACT

Abstract Metazoan oxidative phosphorylation (OXPHOS) complexes are composed of subunits encoded by mitochondrial and nuclear genes, requiring continuous mitonuclear coevolution to ensure functional compatibility. However, mitochondrial and nuclear genomes exhibit separate inheritance patterns, leading to their distinct or even conflicting evolutionary histories. This study aimed to analyse phylogenetic signals among mitochondrial genes, nuclear-encoded OXPHOS genes, and general nuclear genes across 53 beetle species. Two major cases of mitonuclear discordance were detected. The nuclear-encoded OXPHOS genes supported mitochondrial phylogenetic signals in noterids, indicating that in noterids the evolutionary history of OXPHOS complexes diverged from the phylogenetic history. Conversely, nuclear-encoded OXPHOS genes aligned with the phylogenetic history of rhysodines, and this mitonuclear discordance suggests that mitochondrial genomes exhibited clear signatures of genetic introgression. By integrating phylogenetic reconstructions and reticulate evolutionary network analyses, we attributed the mitonuclear discordance in noterids to incomplete lineage sorting. In contrast, the mitochondrial genomes of rhysodines underwent introgressive hybridization events. Although mitonuclear incompatibility is typically resolved by nuclear compensatory mechanisms, our findings indicate that nuclear compensation exhibits limited efficacy at the gene level, yet locally adaptive residues persist. This was further supported by the weak correlation between nuclear-encoded OXPHOS genes and mitochondrial genes, with no robust mitonuclear coevolutionary signals detected. These findings collectively suggest a loose mitonuclear interaction in beetles. The decoupling of mitochondrial and nuclear evolutionary trajectories may serve as an evolutionary “buffer” to accommodate genomic conflicts while maintaining essential OXPHOS systems.

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