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490 News & Comment have much smaller mtDNAs (i.e. animals). Species that exhibit isogamy, such as Chlamydomonas, are an exception to this rule – because both male and female gametes must be motile, there is no asymmetry in selective pressure. Species, such as the mussel Mytilus californianus, where paternal and maternal inheritance of mtDNA occurs, should also be buffered from this effect, because paternal inheritance provides an opportunity for selection to act on the male lineage to purge deleterious mtDNA mutations. Some support does exist for this view. For example, although the male and female mtDNAs of Mytilus possess the same genes, they show striking sequence variation, perhaps as a consequence of the very different selective forces acting on mtDNA in males and females8. Although undoubtedly not the whole story, selection asymmetry provides a plausible framework to explain why the nucleus is the preferred location for organellar genes and why the rates of gene transfer differ between taxa4. Neil J. Gemmell* Dept of Zoology, University of Canterbury, Christchurch, New Zealand. *e-mail: [email protected] Tamsin L. Braisher Landcare Research, PO Box 69, Lincoln, New Zealand. References 1 Selosse, M.A. et al. (2001) Reducing the genome size of organelles favours gene transfer to the nucleus. Trends Ecol. Evol. 16, 135–141 2 Martin, W. and Herrmann, R.G. (1998) Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiol. 118, 9–17 3 Berg, O.G. and Kurland, C.G. (2000) Why mitochondrial genes are most often found in nuclei. Mol. Biol. Evol. 17, 951–961 4 Blanchard, J.L. and Lynch, M. (2000) Organellar genes – why do they end up in the nucleus? Trends Genet. 16, 315–320 5 Ruiz-Pesini, E. et al. (2000) Human mtDNA haplogroups associated with high or reduced spermatozoa motility. Am. J. Hum. Genet. 67, 682–696 6 Frank, S.A. and Hurst, L.D. (1996) Mitochondria and male disease. Nature 383, 224 7 Gemmell, N.J. and Allendorf, F.W. (2001) Mitochondrial mutations may decrease population viability. Trends Ecol. Evol. 16, 115–117 8 Beagley, C.T. et al.(1997) Gender-associated diverse mitochondrial DNA molecules of the mussel Mytilus californianus. Curr. Genet. 31, 318–324 http://tree.trends.com TRENDS in Ecology & Evolution Vol.16 No.9 September 2001 Organelle genome evolution Response from Selosse, Albert and Godelle Gemmell and Braisher argue that selection asymmetry could favour the movement of mitochondrial genes to the nucleus. We agree that their proposal can be added, together with other hypotheses, such as Muller’s ratchet and the high mutagenicity of free radicals1, to selective pressures that, in some but not all lineages, contribute to genetic erosion of organelles. However, their hypothesis is restricted to: (1) uniparentally inherited organelles, which is not a general case2,3; (2) anisogamous species where the gamete responsible for organelle inheritance is not the mobile one; and (3) energy-providing organelles, that is, mitochondria. Plants could nevertheless be an exception to this rule, because, although the male function strongly depends on mitochondrial integrity4, the maternally inherited mitochondria have very large mitochondrial DNA (mtDNA). In addition, the process of genome erosion in organelles is observed independently of organelle phylogenetic origin or function. We argue that intracellular selection, such as competition among genomic molecules or organelles favouring smaller, fastreplicating genomes, is a universal phenomenon for all organelles. Gemmell and Braisher’s proposal emphasizes the need for further studies, mainly modelling, to assess the respective role of these various hypotheses. Such a model would necessarily assume quantitative values for parameters for which we have little information. We think that its predictive power would be restricted to testing for simple evolutionary scenarios. For example, an attractive idea proposed by Gemmell and Braisher is that bi-uniparental inheritance, as observed in the mussel Mytilus edulis, could have been related to the purging of malespecific deleterious mutations of mtDNA. Elaborating more on this, we propose that a nuclear modifier of mtDNA inheritance that acts in the zygote, causing it to retain only the mtDNA from the parent of the same sex as the zygote, could be selected for. In a species where mtDNA inheritance would first be maternal, one would observe a loss of fertility in some males, because they receive male-specific deleterious mitochondrial mutations from their mother. These mutations will thus accumulate slowly, reaching high frequencies. In such a polymorphic population, the mtDNA present in a male functional gamete is unlikely to be malespecifically deleterious. Any nuclear modifier that acts in the male zygote to favour the retention of mtDNA transmitted by the male parent, will confer an advantage by protecting the zygote from inheriting male-specific deleterious mtDNA. At the same time, this modifier does not expose its female carriers to the danger of biparental organelle inheritance sensu Hastings5 (risk of mixing selfish and nonselfish mtDNA): bi-uniparental inheritance would thus be an elegant evolutionary solution against the accumulation of any kind of deleterious mutations, either selfish or sex specific. Marc-André Selosse* Institut de Systématique, Muséum National d’Histoire Naturelle, 43 rue Cuvier, F-75005 Paris, France. *e-mail: [email protected] Béatrice Albert Laboratoire Ecologie, Systématique et Evolution, Université Paris-Sud – bât. 362, 91405 Orsay Cedex, France. Bernard Godelle Laboratoire Génome, Populations, Interactions, Université de Montpellier II – cc 063, F-34095 Montpellier Cedex 05, France. References 1 Selosse, M.A. et al. (2001) Reducing the genome size of organelles favours gene transfer to the nucleus. Trends Ecol. Evol. 16, 135–141 2 Birky, C.W. (1995) Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc. Natl. Acad. Sci. U. S. A. 92, 11331–11338 3 Ankel-Simons, F. and Cummins, J.M. (1996) Misconception about mitochondria and mammalian fertilization: implications for theories on human evolution. Proc. Natl. Acad. Sci. U. S. A. 93, 13859–13863 4 Sabar, M. et al. (1998) Mitochondrial complex I dysfunction: compatibility with survival and reproduction in cytoplasmic and nuclear malesterile mutants of Nicotiana sylvestris. In Proceedings of the 5th International Congress of Plant Mitochondria (Moller, I.M. et al., eds), pp. 87–90, Backhuys Publishers 5 Hastings, I. M. (1992) Population genetics aspects of deleterious cytoplasmic genomes and their effect on the evolution of sexual reproduction. Genet. Res. 59, 215–225 0169-5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved.