Differential fitness of mitochondrial DNA in perturbation cage studies correlates with global abundance and population history in<i>Drosophila simulans</i>

Ballard, J. William O.; James, Andrew

doi:10.1098/rspb.2004.2709

Cited by 36 publications

(38 citation statements)

References 42 publications

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“…Second, population cage studies with these mtDNAs indicate that Dsim mtDNA is indeed selected against relative to Dmel mtDNA (D. Rand, unpublished results). Moreover, less-diverged mtDNA haplotypes within D. simulans show repeatable differences in fitness effects of mtDNA (James and Ballard 2003;Ballard and James 2004). While these arguments do not establish that Dmel and Dsim mtDNA are non-neutral for longevity, it seems plausible that if mtDNA effects are detectable at an early age, there should be some additive mtDNA effects for these haplotypes at a later age when selection is less likely to have influenced their evolution.…”

Section: Discussionmentioning

confidence: 99%

Nuclear–Mitochondrial Epistasis and Drosophila Aging: Introgression of Drosophila simulans mtDNA Modifies Longevity in D. melanogaster Nuclear Backgrounds

2006

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Under the mitochondrial theory of aging, physiological decline with age results from the accumulated cellular damage produced by reactive oxygen species generated during electron transport in the mitochondrion. A large body of literature has documented age-specific declines in mitochondrial function that are consistent with this theory, but relatively few studies have been able to distinguish cause from consequence in the association between mitochondrial function and aging. Since mitochondrial function is jointly encoded by mitochondrial (mtDNA) and nuclear genes, the mitochondrial genetics of aging should be controlled by variation in (1) mtDNA, (2) nuclear genes, or (3) nuclear-mtDNA interactions. The goal of this study was to assess the relative contributions of these factors in causing variation in Drosophila longevity. We compared strains of flies carrying mtDNAs with varying levels of divergence: two strains from Zimbabwe (,20 bp substitutions between mtDNAs), strains from Crete and the United States (20-40 bp substitutions between mtDNAs), and introgression strains of Drosophila melanogaster carrying mtDNA from Drosophila simulans in a D. melanogaster Oregon-R chromosomal background (.500 silent and 80 amino acid substitutions between these mtDNAs). Longevity was studied in reciprocal cross genotypes between pairs of these strains to test for cytoplasmic (mtDNA) factors affecting aging. The intrapopulation crosses between Zimbabwe strains show no difference in longevity between mtDNAs; the interpopulation crosses between Crete and the United States show subtle but significant differences in longevity; and the interspecific introgression lines showed very significant differences between mtDNAs. However, the genotypes carrying the D. simulans mtDNA were not consistently short-lived, as might be predicted from the disruption of nuclear-mitochondrial coadaptation. Rather, the interspecific mtDNA strains showed a wide range of variation that flanked the longevities seen between intraspecific mtDNAs, resulting in very significant nuclear 3 mtDNA epistatic interaction effects. These results suggest that even ''defective'' mtDNA haplotypes could extend longevity in different nuclear allelic backgrounds, which could account for the variable effects attributable to mtDNA haplogroups in human aging.

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Section: Discussionmentioning

confidence: 99%

Nuclear–Mitochondrial Epistasis and Drosophila Aging: Introgression of Drosophila simulans mtDNA Modifies Longevity in D. melanogaster Nuclear Backgrounds

2006

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“…A similar method has been used for estimating changes in frequencies of mitochondrial haplotype in Drosophila (Ballard & James 2004). All analyses were conducted in JMP v. 4.0.3 (SAS Institute, Inc.).…”

Section: (C) Population Cagesmentioning

confidence: 99%

Population dynamics of defensive symbionts in aphids

et al. 2007

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Vertically transmitted micro-organisms can increase in frequency in host populations by providing net benefits to hosts. While laboratory studies have identified diverse beneficial effects conferred by inherited symbionts of insects, they have not explicitly examined the population dynamics of mutualist symbiont infection within populations. In the pea aphid, Acyrthosiphon pisum, the inherited facultative symbiont, Hamiltonella defensa, provides protection against parasitism by the wasp, Aphidius ervi. Despite a high fidelity of vertical transmission and direct benefits of infection accruing to parasitized aphids, Hamiltonella remains only at intermediate frequencies in natural populations. Here, we conducted population cage experiments to monitor the dynamics of Hamiltonella and of another common A. pisum symbiont, Serratia symbiotica, in the presence and absence of parasitism. We also conducted fitness assays of Hamiltonellainfected aphids to search for costs to infection in the absence of parasitism. In the population cages, we found that the frequency of A. pisum infected with Hamiltonella increased dramatically after repeated exposure to parasitism by A. ervi, indicating that selection pressures from natural enemies can lead to the increase of particular inherited symbionts in insect populations. In our laboratory fitness assays, we did not detect a cost to infection with Hamiltonella, but in the population cages not exposed to parasitism, we found a significant decline in the frequency of both Hamiltonella and Serratia. The declining frequencies of Hamiltonella-infected aphids in population cages in the absence of parasitism indicate a probable cost to infection and may explain why Hamiltonella remains at intermediate frequencies in natural populations.

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“…This implies that siIII males are more bioenergetically efficient than those with siII mtDNA. This result is in conflict with the observations that siII flies are more successful than siIII flies in nature and in laboratory studies (Dean et al, 2003;Ballard and James, 2004;Satta et al, 1988). If the efficiency of mitochondrial metabolism is related to organismal success there are at least six potential reasons for the observed conflict.…”

Section: Discussionmentioning

confidence: 66%

“…They demonstrated that the three mitotypes have unequal ability to out compete the host mtDNA type (siII>-III>-I). Ballard and James (2004) showed the same rank order of mtDNA fitness in laboratory perturbation cages. James and Ballard (2003) used the reciprocal introgression approach to show differences in three life-history traits.…”

Section: Introductionmentioning

confidence: 71%

Sympatric Drosophila simulans flies with distinct mtDNA show age related differences in mitochondrial metabolism

Katewa

Ballard

2007

Insect Biochemistry and Molecular Biology

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The primary causes of age related changes in mitochondrial metabolism are not known. The goal of this study is to document the influence of naturally occurring mtDNA variation on age dependent changes in mitochondrial respiration, hydrogen peroxide (H 2 O 2 ) generation and antioxidant defenses in the fly Drosophila simulans. Possible changes include an increase in rates of reactive oxygen species production with age and/or an age dependent decrease in antioxidant response. For this study we have used flies harboring distinct siII and siIII mtDNA types. Previously we have shown that males harboring siII mtDNA had higher rates 30 of mitochondrial H 2 O 2 production from complex III at 11 d compared to males with the siIII mtDNA type. Here, we corroborate those results and show that Drosophila harboring the siII and siIII mtDNA types exhibit significantly different patterns of pro-oxidant and antioxidant activities as they age. Flies harboring siII mtDNA had higher rates of mitochondrial H 2 O 2 production and manganese superoxide dismutase activity at 11 and 18 d of age than siIII mtDNA 35 harboring flies. Copper-zinc superoxide dismutase activity increased from 11 to 25 d in siII flies while the accumulation of oxidized glutathione did not change between 11 and 25 d. In contrast, siIII harboring flies showed an age dependent increase in H 2 O 2 production, reaching higher production rates on day 25 than that observed in siII flies. Copper-zinc superoxide dismutase activities did not change between 11 and 25 d while the oxidized glutathione accumulation increased with age. The results show antioxidant levels correlate with pro-oxidant levels in siII but not siIII flies. These results demonstrate our ability to correlate mtDNA variation with differences in whole mitochondrial physiology and individual complex biochemistry.

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

Cited by 36 publications

References 42 publications

Nuclear–Mitochondrial Epistasis and Drosophila Aging: Introgression of Drosophila simulans mtDNA Modifies Longevity in D. melanogaster Nuclear Backgrounds

Nuclear–Mitochondrial Epistasis and Drosophila Aging: Introgression of Drosophila simulans mtDNA Modifies Longevity in D. melanogaster Nuclear Backgrounds

Population dynamics of defensive symbionts in aphids

Sympatric Drosophila simulans flies with distinct mtDNA show age related differences in mitochondrial metabolism

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