Population genetics of the cytoplasm and the units of selection on mitochondrial DNA in <Emphasis Type="Italic">Drosophila melanogaster</Emphasis> |
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Authors: | David M Rand |
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Institution: | (1) Department of Ecology and Evolution, Brown University, Providence, RI 02912, USA |
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Abstract: | Biological variation exists across a nested set of hierarchical levels from nucleotides within genes to populations within
species to lineages within the tree of life. How selection acts across this hierarchy is a long-standing question in evolutionary
biology. Recent studies have suggested that genome size is influenced largely by the balance of selection, mutation and drift
in lineages with different population sizes. Here we use population cage and maternal transmission experiments to identify
the relative strength of selection at an individual and cytoplasmic level. No significant trends were observed in the frequency
of large (L) and small (S) mtDNAs across 14 generations in population cages. In all replicate cages, new length variants were
observed in heteroplasmic states indicating that spontaneous length mutations occurred in these experimental populations.
Heteroplasmic flies carrying L genomes were more frequent than those carrying S genomes suggesting an asymmetric mutation
dynamic from larger to smaller mtDNAs. Mother-offspring transmission of heteroplasmy showed that the L mtDNA increased in
frequency within flies both between and within generations despite sampling drift of the same intensity as occurred in population
cages. These results suggest that selection for mtDNA size is stronger at the cytoplasmic than at the organismal level. The
fixation of novel mtDNAs within and between species requires a transient intracellular heteroplasmic stage. The balance of
population genetic forces at the cytoplasmic and individual levels governs the units of selection on mtDNA, and has implications
for evolutionary inference as well as for the effects of mtDNA mutations on fitness, disease and aging. |
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