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 1 . Contrastingly, matchups between distant 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 revealed that the non-coding region, containing origins of replication, governs selfish transmission. Uniparental inheritance prevents encounters between distantly related genomes. Nonetheless, within 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.Natural selection culls populations of compromising mutations and favors traits that enhance organismal fitness. Nuclear genes have a relatively uniform exposure to natural selection as a result of regimented replication and segregation. In contrast, unconstrained competition among multiple mitochondrial genomes creates alternative ways to select for fit genomes, as well as opportunities for selfish genomes to increase in abundance.In heteroplasmic lines of Drosophila, mitochondrial genomes harboring mutations detrimental to oxidative phosphorylation (OXPHOS) function suffered a transmission disadvantage, even when complemented by co-resident wild-type genomes. The resulting Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial_policies/license.html#terms 2 Correspondence to: Patrick H. O'Farrell, ofarrell@cgl.ucsf.edu.
Accession CodesThe complete sequence of a recombinant mitochondrial genome (Supplementary Figure 1a) between the two parental genomes (ATP6[1] and mt:ND2 del1 + mt:CoI T300I ) was deposited in Genbank and given the following accession number: KU764535.
Author Contributions
Competing financial interestsThe authors declare no competing financial interests. [6][7][8] . In multicellular organisms, defective mitochondrial genomes carried in animals can also benefit from selfish drive to enhance their propagation 9-14 .
HHS Public AccessTo study head-to-head competition between mitochondrial genomes, we used cytoplasmic transplantation to bypass uniparental inheritance, which normally prevents encounters between unrelated genomes. In the resulting heteroplasmic lines, purifying selection dominated competition ...