Original Article

Heredity (2013) 110, 57–62; doi:10.1038/hdy.2012.60; published online 26 September 2012

Paternal transmission of mitochondrial DNA as an integral part of mitochondrial inheritance in metapopulations of Drosophila simulans

J N Wolff1,2, M Nafisinia1,4, P Sutovsky3 and J W O Ballard1,2

  1. 1School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, New South Wales, Australia
  2. 2Evolution and Ecology Research Centre, University of New South Wales, Sydney, New South Wales, Australia
  3. 3Division of Animal Sciences, Department of Obstetrics, Gynecology and Women’s Health, University of Missouri, Columbia, MO, USA

Correspondence: Dr JN Wolff, School of Biotechnology and Biomolecular Sciences, The University of New South Wales, Sydney, New South Wales 2052, Australia. E-mail: jonciwolff@yahoo.com

4Joint first author.

Received 8 March 2012; Revised 8 July 2012; Accepted 8 August 2012
Advance online publication 26 September 2012

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Abstract

Maternal inheritance is one of the hallmarks of animal mitochondrial DNA (mtDNA) and central to its success as a molecular marker. This mode of inheritance and subsequent lack of heterologous recombination allows us to retrace evolutionary relationships unambiguously down the matriline and without the confounding effects of recombinant genetic information. Accumulating evidence of biparental inheritance of mtDNA (paternal leakage), however, challenges our current understanding of how this molecule is inherited. Here, using Drosophila simulans collected from an East African metapopulation exhibiting recurring mitochondrial heteroplasmy, we conducted single fly matings and screened F1 offspring for the presence of paternal mtDNA using allele-specific PCR assays (AS–PCR). In all, 27 out of 4092 offspring were identified as harboring paternal mtDNA, suggesting a frequency of 0.66% paternal leakage in this species. Our findings strongly suggest that recurring mtDNA heteroplasmy as observed in natural populations of Drosophila simulans is most likely caused by repeated paternal leakage. Our findings further suggest that this phenomenon to potentially be an integral part of mtDNA inheritance in these populations and consequently of significance for mtDNA as a molecular marker.

Keywords:

mtDNA; paternal leakage; biparental inheritance; heteroplasmy; mitochondria