Evidence for non-neutrality of mitochondrial DNA haplotypes in Drosophila pseudoobscura.

Abstract

Mitochondrial DNA (mtDNA) haplotypes usually are assumed to be neutral, unselected markers of evolving female lineages. This assumption was tested by monitoring haplotype frequencies in 12 experimental populations of Drosophila pseudoobscura which were polymorphic for mtDNA haplotypes. Populations were maintained for at least 10 generations, and in one case for 32 generations, while tests of mtDNA selective neutrality were conducted. In an initial population, formed from a mixture of two strains with different mitochondrial haplotypes, the frequency of the Bogota haplotype increased 46% in 3 generations, reaching an apparent equilibrium frequency of 82% after 32 generations. Perturbation of this equilibrium by addition of the less common haplotype resulted in a rapid, dramatic increase in frequency of the second haplotype, and a return to essentially the same equilibrium frequency as before perturbation. This behavior is not consistent with mtDNA neutrality, nor is the equilibrium consistent with a simple model of constant selection on the haploid mtDNAs. Replicate cage experiments with mtDNA haplotypes did not always generate the same result as the initial cage. Several lines of evidence, including manipulations of the nuclear genome, support the idea that both nuclear and mitochondrial genomes are involved in the dramatic mtDNA frequency changes. In another experiment, strong female viability selection was implicated via mtDNA frequency changes. Although the causes of the dramatic mtDNA frequency changes in our populations are not obvious, it is clear that Drosophila mitochondrial haplotypes are not always simply neutral markers. Our findings are relevant to the introduction of a novel mtDNA variant from one species or one population into another. Such introductions could be strongly favored by selection, even if it is sporadic.

Differential fitness of mitochondrial DNA in perturbation cage studies correlates with global abundance and population history inDrosophila simulans

“…Population cage studies using Drosophila have provided evidence that mtDNA can influence the frequency of flies in cages. In D. pseudoobscura it has been suggested that the apparent 'non-neutral' behaviour of mtDNA types (MacRae & Anderson 1988) is due to mating incompatibility (Singh & Hale 1990;but see MacRae & Anderson 1990;Jenkins et al 1996). In D. subobscura, frequency shifts of mtDNAs have been observed in population cages (Fos et al 1990), but the cages were not replicated and the lines used had complex chromosomal inversions that may have influenced fly fitness.…”

Testing Neutrality of mtDNA Using Multigeneration Cytonuclear Data

“…In addition to the above results, a number of recent experiments suggest apparent non-neutral behaviors of mtDNA markers (Clark and Lyckegaard, 1988;MacRae and Anderson 1988;Fos et al, 1990;Nigro and Prout, 1990;Pollak, 1991;Arnason, 1991;Kambhampati et al, 1992;Scribner and Avise, 1994a, b;Hutter and Rand, 1995;etc.). Singh and Hale (1990) suggested that the apparent "non-neutral" behavior may also be caused by mating preference and that any attempt to understand the role of selection on mtDNA variants should first begin with simpler conspecific variants rather than with interspecific variants; however see Anderson (1990), Jenkins et al (1996).…”

Ecology, the pace‐of‐life, epistatic selection and the maintenance of genetic variation in life‐history genes

“…However, recent research has associated mtDNA polymorphism with key rate-dependent LH and related phenotypes, such as development time (Christie et al, 2004;Erić et al, 2022), longevity (Jelić et al, 2015), stress resistance (Jelić et al, 2015;Sun et al, 2019), general activity (Ueno & Takahashi, 2021) and even metabolic rate (Baris et al, 2017;Đorđević et al, 2016;Kurbalija Novičić et al, 2015). Second, observations such as those of stable mtDNA haplotype frequencies over time and space (Andrianov et al, 2008;Oliver et al, 2005) MacRae & Anderson, 1988;Oliver et al, 2005).…”