Germline Bottlenecks and the Evolutionary Maintenance of Mitochondrial Genomes

,a

Corresponding author: Jonathan Pritchard, Department of Biological Sciences, Stanford University, Stanford, CA 94305., jkp{at}charles.stanford.edu (E-mail).

Communicating editor: A. G. CLARK

Several features of the biology of mitochondria suggest that mitochondria might be susceptible to Muller's ratchet and other forms of evolutionary degradation: Mitochondria have predominantly uniparental inheritance, appear to be nonrecombining, and have high mutation rates producing significant deleterious variation. We demonstrate that the persistence of mitochondria may be explained by recent data that point to a severe "bottleneck" in the number of mitochondria passing through the germline in humans and other mammals. We present a population-genetic model in which deleterious mutations arise within individual mitochondria, while selection operates on assemblages of mitochondria at the level of their eukaryotic hosts. We show that a bottleneck increases the efficacy of selection against deleterious mutations by increasing the variance in fitness among eukaryotic hosts. We investigate both the equilibrium distribution of deleterious variation in large populations and the dynamics of Muller's ratchet in small populations. We find that in the absence of the ratchet, a bottleneck leads to improved mitochondrial performance and that, over a longer time scale, a bottleneck acts to slow the progression of the ratchet.

This article has been cited by other articles:

				R. J. Soderberg and O. G. Berg Mutational Interference and the Progression of Muller's Ratchet When Mutations Have a Broad Range of Deleterious Effects Genetics, October 1, 2007; 177(2): 971 - 986. [Abstract] [Full Text] [PDF]

				D. Roze, F. Rousset, and Y. Michalakis Germline Bottlenecks, Biparental Inheritance and Selection on Mitochondrial Variants: A Two-Level Selection Model Genetics, July 1, 2005; 170(3): 1385 - 1399. [Abstract] [Full Text] [PDF]

				J. Van Blerkom Mitochondria in human oogenesis and preimplantation embryogenesis: engines of metabolism, ionic regulation and developmental competence Reproduction, September 1, 2004; 128(3): 269 - 280. [Abstract] [Full Text] [PDF]

				R. T. Cox and A. C. Spradling A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis Development, April 15, 2003; 130(8): 1579 - 1590. [Abstract] [Full Text] [PDF]

				I. Gordo, A. Navarro, and B. Charlesworth Muller's Ratchet and the Pattern of Variation at a Neutral Locus Genetics, June 1, 2002; 161(2): 835 - 848. [Abstract] [Full Text] [PDF]

				D. R. Taylor, C. Zeyl, and E. Cooke Conflicting levels of selection in the accumulation of mitochondrial defects in Saccharomyces cerevisiae PNAS, March 19, 2002; 99(6): 3690 - 3694. [Abstract] [Full Text] [PDF]

				D. C. Krakauer and J. B. Plotkin Redundancy, antiredundancy, and the robustness of genomes PNAS, January 24, 2002; (2002) 32668599. [Abstract] [Full Text] [PDF]

				D. J. Funk, J. J. Wernegreen, and N. A. Moran Intraspecific Variation in Symbiont Genomes: Bottlenecks and the Aphid-Buchnera Association Genetics, February 1, 2001; 157(2): 477 - 489. [Abstract] [Full Text]

				C. G. Kurland and S. G. E. Andersson Origin and Evolution of the Mitochondrial Proteome Microbiol. Mol. Biol. Rev., December 1, 2000; 64(4): 786 - 820. [Abstract] [Full Text] [PDF]

				D. M. Weinreich and D. M. Rand Contrasting Patterns of Nonneutral Evolution in Proteins Encoded in Nuclear and Mitochondrial Genomes Genetics, September 1, 2000; 156(1): 385 - 399. [Abstract] [Full Text]

				A. Sekowska, A. Danchin, and J.-L. Risler Phylogeny of related functions: the case of polyamine biosynthetic enzymes Microbiology, August 1, 2000; 146(8): 1815 - 1828. [Abstract] [Full Text]

				D. C. Krakauer and J. B. Plotkin Redundancy, antiredundancy, and the robustness of genomes PNAS, February 5, 2002; 99(3): 1405 - 1409. [Abstract] [Full Text] [PDF]