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

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barnacles, including three newly sequenced and one previously unpublished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.