Extensive paternal mtDNA leakage in natural populations of Drosophila melanogaster

Strict maternal inheritance is considered a hallmark of animal mtDNA. Although recent reports suggest that paternal leakage occurs in a broad range of species, it is still considered an exceptionally rare event. To evaluate the impact of paternal leakage on the evolution of mtDNA, it is essential to...

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Bibliographic Details
Published in:Molecular ecology 2013-04, Vol.22 (8), p.2106-2117
Main Authors: Nunes, Maria D. S., Dolezal, Marlies, Schlötterer, Christian
Format: Article
Language:English
Subjects:
Animals
Biological and medical sciences
Biological evolution
DNA, Mitochondrial - genetics
Drosophila melanogaster
Drosophila melanogaster - genetics
Evolutionary biology
Female
Fundamental and applied biological sciences. Psychology
Genetic Variation
Genetics of eukaryotes. Biological and molecular evolution
Haplotypes
Heredity
heteroplasmy
Mitochondrial DNA
Models, Theoretical
Molecular Sequence Data
mtDNA diversity
Original
paternal leakage
Population - genetics
Population genetics, reproduction patterns
recombination
Recombination, Genetic
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Summary:Strict maternal inheritance is considered a hallmark of animal mtDNA. Although recent reports suggest that paternal leakage occurs in a broad range of species, it is still considered an exceptionally rare event. To evaluate the impact of paternal leakage on the evolution of mtDNA, it is essential to reliably estimate the frequency of paternal leakage in natural populations. Using allele‐specific real‐time quantitative PCR (RT‐qPCR), we show that heteroplasmy is common in natural populations with at least 14% of the individuals carrying multiple mitochondrial haplotypes. However, the average frequency of the minor mtDNA haplotype is low (0.8%), which suggests that this pervasive heteroplasmy has not been noticed before due to a lack of power in sequencing surveys. Based on the distribution of mtDNA haplotypes in the offspring of heteroplasmic mothers, we found no evidence for strong selection against one of the haplotypes. We estimated that the rate of paternal leakage is 6% and that at least 100 generations are required for complete sorting of mtDNA haplotypes. Despite the high proportion of heteroplasmic individuals in natural populations, we found no evidence for recombination between mtDNA molecules, suggesting that either recombination is rare or recombinant haplotypes are counter‐selected. Our results indicate that evolutionary studies using mtDNA as a marker might be biased by paternal leakage in this species.
ISSN:0962-1083
1365-294X
DOI:10.1111/mec.12256