title: Selfish little circles: transmission bias and evolution of large deletion-bearing mitochondrial DNA in Caenorhabditis briggsae nematodes.
abstract: Selfish DNA poses a significant challenge to genome stability and organismal fitness in diverse eukaryotic lineages. Although selfish mitochondrial DNA (mtDNA) has known associations with cytoplasmic male sterility in numerous gynodioecious plant species and is manifested as petite mutants in experimental yeast lab populations, examples of selfish mtDNA in animals are less common. We analyzed the inheritance and evolution of mitochondrial DNA bearing large heteroplasmic deletions including nad5 gene sequences (nad5Δ mtDNA), in the nematode Caenorhabditis briggsae. The deletion is widespread in C. briggsae natural populations and is associated with deleterious organismal effects. We studied the inheritance patterns of nad5Δ mtDNA using eight sets of C. briggsae mutation-accumulation (MA) lines, each initiated from a different natural strain progenitor and bottlenecked as single hermaphrodites across generations. We observed a consistent and strong drive toward higher levels of deletion-bearing molecules in the heteroplasmic pool of mtDNA after ten generations of bottlenecking. Our results demonstrate a uniform transmission bias whereby nad5Δ mtDNA accumulates to higher levels relative to intact mtDNA in multiple genetically diverse natural strains of C. briggsae. We calculated an average 1% per-generation transmission bias for deletion-bearing mtDNA relative to intact genomes. Our study, coupled with known deleterious phenotypes associated with high deletion levels, shows that nad5Δ mtDNA are selfish genetic elements that have evolved in natural populations of C. briggsae, offering a powerful new system to study selfish mtDNA dynamics in metazoans.
authors.affiliation: Department of Zoology and Center for Genome Research and Biocomputing, Oregon State University, Corvallis, Oregon, United States of America.
authors.forename: Katie A
authors.initials: KA
authors.lastname: Clark
authors.forename: Dana K
authors.initials: DK
authors.lastname: Howe
authors.forename: Kristin
authors.initials: K
authors.lastname: Gafner
authors.forename: Danika
authors.initials: D
authors.lastname: Kusuma
authors.forename: Sita
authors.initials: S
authors.lastname: Ping
authors.forename: Suzanne
authors.initials: S
authors.lastname: Estes
authors.forename: Dee R
authors.initials: DR
authors.lastname: Denver
mesh_terms: D000818:Animals; D002107:Caenorhabditis / Q000235:genetics*; D004270:DNA, Circular / Q000235:genetics / Q000378:metabolism; D018509:DNA, Helminth / Q000235:genetics* / Q000378:metabolism; D004272:DNA, Mitochondrial / Q000235:genetics* / Q000378:metabolism; D019143:Evolution, Molecular; D017353:Gene Deletion; D015801:Helminth Proteins / Q000235:genetics; D008969:Molecular Sequence Data; D009245:NADH Dehydrogenase / Q000235:genetics; D012091:Repetitive Sequences, Nucleic Acid; D017422:Sequence Analysis, DNA
chemical_list: D004270:DNA, Circular; D018509:DNA, Helminth; D004272:DNA, Mitochondrial; D015801:Helminth Proteins; D009245:NADH Dehydrogenase