Drosophila mitotypes determine developmental time in a diet and temperature dependent manner

Towarnicki, Samuel G.; Ballard, J. William O.

doi:10.1016/j.jinsphys.2017.06.002

Cited by 9 publications

(18 citation statements)

References 74 publications

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“…Here, we have shown that flies harbouring Alstonville and Dahomey mtDNA have a reciprocal fitness advantage when fed the 1:2 P:C and 1:16 P:C diets. The flip in fitness advantage was caused by changes in larval development time and resulted in significant disparities in the number of flies eclosing in 3 d. Towarnicki and Ballard [ 15 ] previously reported similar differences in larval development at 23° C and 27° C. Interestingly, however, these differences were lost when larvae were raised at 19° C. Larval development strategies are likely important in nature and have been the subject of multiple experimental evolution studies aimed at understanding the evolutionary strategies associated with adaptations to heterogeneous food supplies [ 59 , 60 ]. Differences in larval diet have recently been shown to influence adult metabolism and lifespan [ 61 ].…”

Section: Resultsmentioning

confidence: 99%

“…There are also three rRNA differences (two srRNA and one lrRNA) [ 83 ] and 52 A+T-rich region variations [ 84 ] ( S1 Table ). Towarnicki and Ballard [ 15 ] mapped the two srRNA mutations on the human mitoribosome and proposed that they are unlikely to influence mitochondrial function [ 83 , 85 ] so they are not considered here. Selection has rarely been shown to act on the mitochondrial A+T rich or control region [but see, 21 , 27 ], and no differences were identified in secondary structures or the central T-stretch between the Alstonville and Dahomey mitotypes [ 15 ].…”

Section: Resultsmentioning

confidence: 99%

“…Towarnicki and Ballard [ 15 ] mapped the two srRNA mutations on the human mitoribosome and proposed that they are unlikely to influence mitochondrial function [ 83 , 85 ] so they are not considered here. Selection has rarely been shown to act on the mitochondrial A+T rich or control region [but see, 21 , 27 ], and no differences were identified in secondary structures or the central T-stretch between the Alstonville and Dahomey mitotypes [ 15 ]. However, differences in the number of repeats have been recently shown to influence mitochondrial functions [ 86 ].…”

Section: Resultsmentioning

confidence: 99%

“…melanogaster Canton S, a 1:2 Protein: Carbohydrate (P:C) ratio of food yielded the highest egg-laying rate and a 1:16 P:C ratio maximised survival [ 13 ]. Aw et al [ 14 ] and Towarnicki and Ballard [ 15 ] demonstrated a more complex scenario whereby diet interacted with Drosophila mitotype and with other environmental factors such as temperature. For adults, Aw et al [ 14 ] reported sex-specific influences of mitotype and diet on mitochondrial functions and physiological traits in males harbouring the Alstonville and Japan mitotypes.…”

Section: Introductionmentioning

confidence: 99%

“…For adults, Aw et al [ 14 ] reported sex-specific influences of mitotype and diet on mitochondrial functions and physiological traits in males harbouring the Alstonville and Japan mitotypes. In larvae, Towarnicki and Ballard [ 15 ] manipulated food and temperature to study the development of the Alstonville and Dahomey mitotypes. We observed that larvae harbouring the latter mitotype developed more slowly than the former when fed a high protein diet at all temperatures, but more quickly when fed the high carbohydrate diet at higher temperatures.…”

Section: Introductionmentioning

confidence: 99%

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Genotype to phenotype: Diet-by-mitochondrial DNA haplotype interactions drive metabolic flexibility and organismal fitness

Towarnicki

Melvin

et al. 2018

PLoS Genet

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Diet may be modified seasonally or by biogeographic, demographic or cultural shifts. It can differentially influence mitochondrial bioenergetics, retrograde signalling to the nuclear genome, and anterograde signalling to mitochondria. All these interactions have the potential to alter the frequencies of mtDNA haplotypes (mitotypes) in nature and may impact human health. In a model laboratory system, we fed four diets varying in Protein: Carbohydrate (P:C) ratio (1:2, 1:4, 1:8 and 1:16 P:C) to four homoplasmic Drosophila melanogaster mitotypes (nuclear genome standardised) and assayed their frequency in population cages. When fed a high protein 1:2 P:C diet, the frequency of flies harbouring Alstonville mtDNA increased. In contrast, when fed the high carbohydrate 1:16 P:C food the incidence of flies harbouring Dahomey mtDNA increased. This result, driven by differences in larval development, was generalisable to the replacement of the laboratory diet with fruits having high and low P:C ratios, perturbation of the nuclear genome and changes to the microbiome. Structural modelling and cellular assays suggested a V161L mutation in the ND4 subunit of complex I of Dahomey mtDNA was mildly deleterious, reduced mitochondrial functions, increased oxidative stress and resulted in an increase in larval development time on the 1:2 P:C diet. The 1:16 P:C diet triggered a cascade of changes in both mitotypes. In Dahomey larvae, increased feeding fuelled increased β-oxidation and the partial bypass of the complex I mutation. Conversely, Alstonville larvae upregulated genes involved with oxidative phosphorylation, increased glycogen metabolism and they were more physically active. We hypothesise that the increased physical activity diverted energy from growth and cell division and thereby slowed development. These data further question the use of mtDNA as an assumed neutral marker in evolutionary and population genetic studies. Moreover, if humans respond similarly, we posit that individuals with specific mtDNA variations may differentially metabolise carbohydrates, which has implications for a variety of diseases including cardiovascular disease, obesity, and perhaps Parkinson’s Disease.

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