Relaxed selection on male mitochondrial genes in DUI bivalves eases the need for mitonuclear coevolution

• Published in: Journal of evolutionary biology Vol. 34; no. 11; pp. 1722 - 1736
• Main Authors: Maeda, Gerald P., Iannello, Mariangela, McConie, Hunter J., Ghiselli, Fabrizio, Havird, Justin C.
• Format: Journal Article
• Language: English
• Published: Switzerland Blackwell Publishing Ltd 01.11.2021
• Subjects: Animals; Bivalvia; Bivalvia - genetics; Coevolution; cytonuclear coevolution; cytonuclear interactions; DNA, Mitochondrial; Eukaryotes; Female; Genes; Genes, Mitochondrial; Genome, Mitochondrial; Genomes; Inheritance Patterns; Inheritances; Male; Maternal inheritance; Mitochondria; mitochondrial respiration; Molecular evolution; Mollusks; mt‐miRNAs; nuclear compensation; Nuclear interactions; ORFans; Positive selection; Residues; Sex; smithRNAs; Species; ORFans; mt-miRNAs; nuclear compensation; cytonuclear coevolution; cytonuclear interactions; mitochondrial respiration; smithRNAs
• ISSN: 1010-061X; 1420-9101
• DOI: 10.1111/jeb.13931

Mitonuclear coevolution is an important prerequisite for efficient energy production in eukaryotes. However, many bivalve taxa experience doubly uniparental inheritance (DUI) and have sex‐specific mitochondrial (mt) genomes, providing a challenge for mitonuclear coevolution. We examined possible mechanisms to reconcile mitonuclear coevolution with DUI. No nuclear‐encoded, sex‐specific OXPHOS paralogs were found in the DUI clam Ruditapes philippinarum, refuting OXPHOS paralogy as a solution in this species. It is also unlikely that mt changes causing disruption of nuclear interactions are strongly selected against because sex‐specific mt‐residues or those under positive selection in M mt genes were not depleted for contacting nuclear‐encoded residues. However, M genomes showed consistently higher dN/dS ratios compared to putatively ancestral F genomes in all mt OXPHOS genes and across all DUI species. Further analyses indicated that this was consistently due to relaxed, not positive selection on M vs. F mt OXPHOS genes. Similarly, selection was relaxed on the F genome of DUI species compared to species with strict maternal inheritance. Coupled with recent physiological and molecular evolution studies, we suggest that relaxed selection on M mt function limits the need to maintain mitonuclear interactions in M genomes compared to F genomes. We discuss our findings with regard to OXPHOS function and the origin of DUI. In many species of bivalves, different mitochondrial genomes undergo sex‐specific inheritance in a process termed doubly‐uniparental inheritance (DUI). In this study, we asked how a single nuclear genome might coevolve with two, sometimes highly divergent mitochondrial genomes in the same species. We found no evidence of sex‐specific, nuclear encoded mt paralogs in DUI species and also no evidence that selection has acted to restrict sex‐specific changes in mtDNA to sites that lack physical nuclear interactions. But mtDNA in males was found to be under highly relaxed selection compared to females. Coupled with recent physiological evidence, we suggest that nuclear coevolution may be may important with female mtDNA compared to male mtDNA in DUI species.