Selfish drive can trump function when animal mitochondrial genomes compete.
Mitochondrial genomes compete for transmission from mother to progeny. We explored this competition by introducing a second genome into Drosophila melanogaster to follow transmission. Competitions between closely related genomes favored those functional in electron transport, resulting in a host-beneficial purifying selection. In contrast, matchups between distantly related genomes often favored those with negligible, negative or lethal consequences, indicating selfish selection. Exhibiting powerful selfish selection, a genome carrying a detrimental mutation displaced a complementing genome, leading to population death after several generations. In a different pairing, opposing selfish and purifying selection counterbalanced to give stable transmission of two genomes. Sequencing of recombinant mitochondrial genomes showed that the noncoding region, containing origins of replication, governs selfish transmission. Uniparental inheritance prevents encounters between distantly related genomes. Nonetheless, in each maternal lineage, constant competition among sibling genomes selects for super-replicators. We suggest that this relentless competition drives positive selection, promoting change in the sequences influencing transmission.
Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, California, USA.
Hansong
H
Ma
Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, California, USA.
Patrick H
PH
O'Farrell
D000818:Animals; D004261:DNA Replication; D004272:DNA, Mitochondrial / Q000235:genetics*; D004331:Drosophila melanogaster / Q000145:classification / Q000235:genetics* / Q000254:growth & development; D019143:Evolution, Molecular; D050259:Genes, Mitochondrial / Q000235:genetics*; D054629:Genome, Mitochondrial / Q000235:genetics*; D009154:Mutation / Q000235:genetics*; D012641:Selection, Genetic / Q000235:genetics*
D004272:DNA, Mitochondrial