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.
Highlights
Deleterious mutations leading to reduced organismal fitness are expected to be eliminated from natural populations due to purifying selection, provided selection is sufficiently strong
Eight C. briggsae natural strains were chosen to serve as progenitor strains to include representatives of the three major intraspecific C. briggsae clades, as well as strains that vary in terms of relevant genotypes at the nad5 locus surveyed here (Figure 1)
Among the 142 MA lines derived from Clade I and II progenitors analyzed, 37 were found to have increased nad5D mitochondrial DNA (mtDNA) levels across ten generations and zero had decreased relative deletion levels that were detectable by our PCR assay
Summary
Deleterious mutations leading to reduced organismal fitness are expected to be eliminated from natural populations due to purifying selection, provided selection is sufficiently strong. Some genetic elements, termed ‘‘selfish’’ or ‘‘parasitic’’ DNA, display transmission advantages and long-term evolutionary persistence despite neutral or negative organismal fitness consequences. Supernumerary chromosomes, segregation distorters, transposable elements, and the cytoplasmic genomes of microorganisms and organelles [1]. Mitochondrial DNA (mtDNA)-encoded and nuclear electron transport chains genes have coevolved in eukaryotes to produce functional electron transport chain complexes, mtDNA underlies cytonuclear conflict and cytoplasmic male sterility in over 150 plant species [2]. Saccharomyces cerevisiae petite mutants, caused by heteroplasmic mtDNA molecules bearing large deletions, were found to predominate in small but not large experimental yeast populations [3]. Selfish mtDNA dynamics have been characterized in species of filamentous fungi [4,5]
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