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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.