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Accelerated mitochondrial genome evolution in parasitic barnacles driven by adaptive and non-adaptive responses

Jung, Jibum1; Song, Siliang2; Kim, Myeong-Yeon1; Kwak, Haena3; Chan, Benny K. K.4; Cha, Sun-Shin1; Hwang, Ui-Wook3; Park, Joong-Ki1

Published Oct 30, 2025 on Dryad. https://doi.org/10.5061/dryad.tx95x6b9w

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Abstract

Parasitic lifestyles often impose profound evolutionary pressures, affecting molecular evolution through both adaptive and non-adaptive mechanisms. Among barnacles (subclass Cirripedia), the obligate parasitic Rhizocephala differ markedly from their filter-feeding thoracican relatives in morphology, ecology, and life history. However, how the shift to parasitism has shaped mitochondrial genome evolution within Cirripedia remains unclear. Here, we present the first comprehensive comparative analysis of mitochondrial genomes between parasitic and non-parasitic barnacles, including three newly sequenced and one previously unpublished species of parasitic Rhizocephala, a clade whose mitochondrial genomes had not been characterized until now. Phylogenomic and molecular evolutionary analyses reveal that Rhizocephala species exhibit extremely long branches, likely attributed to the clade-specific tempo (high substitution rate) and mode (selection pressure) of mtDNA sequence evolution associated with their parasitic lifestyle. A two-cluster molecular clock test reveals significantly elevated substitution rates across rhizocephalans, consistent with reduced effective population sizes (Ne) linked to their opportunistic, host-dependent life cycles. We also detect signatures of positive selection in protein-coding genes encoding key components of the electron transport chain complexes III and IV. Structural modeling highlights amino acid substitutions at functionally critical sites for electron transfer and proton pumping, suggesting adaptive modifications to mitochondrial bioenergetics under hypoxic conditions within host tissues. Together, our findings underscore that both non-adaptive (genetic drift, relaxed selection) and adaptive (positive selection) processes have driven the rapid sequence divergence of mitochondrial genomes in parasitic Rhizocephala. Further experimental study is needed to elucidate how mitochondrial and nuclear-encoded subunits of oxidative phosphorylation coevolve in this specialized parasitic group.