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Sex-specific effects of mitochondrial haplotype on metabolic rate in Drosophila melanogaster support predictions of the Mother's Curse hypothesis

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Sex-specific effects of mitochondrial haplotype on metabolic rate in Drosophila melanogaster support predictions of the Mother's Curse hypothesis. / Nagarajan-Radha, Venkatesh; Aitkenhead, Ian; Clancy, David; Chown, Steven L.; Dowling, Damian K.

In: Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 375, No. 1790, 20190178, 30.01.2020.

Research output: Contribution to Journal/MagazineJournal articlepeer-review

Harvard

Nagarajan-Radha, V, Aitkenhead, I, Clancy, D, Chown, SL & Dowling, DK 2020, 'Sex-specific effects of mitochondrial haplotype on metabolic rate in Drosophila melanogaster support predictions of the Mother's Curse hypothesis', Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 375, no. 1790, 20190178. https://doi.org/10.1098/rstb.2019.0178

APA

Nagarajan-Radha, V., Aitkenhead, I., Clancy, D., Chown, S. L., & Dowling, D. K. (2020). Sex-specific effects of mitochondrial haplotype on metabolic rate in Drosophila melanogaster support predictions of the Mother's Curse hypothesis. Philosophical Transactions of the Royal Society B: Biological Sciences, 375(1790), [20190178]. https://doi.org/10.1098/rstb.2019.0178

Vancouver

Nagarajan-Radha V, Aitkenhead I, Clancy D, Chown SL, Dowling DK. Sex-specific effects of mitochondrial haplotype on metabolic rate in Drosophila melanogaster support predictions of the Mother's Curse hypothesis. Philosophical Transactions of the Royal Society B: Biological Sciences. 2020 Jan 30;375(1790). 20190178. https://doi.org/10.1098/rstb.2019.0178

Author

Nagarajan-Radha, Venkatesh ; Aitkenhead, Ian ; Clancy, David ; Chown, Steven L. ; Dowling, Damian K. / Sex-specific effects of mitochondrial haplotype on metabolic rate in Drosophila melanogaster support predictions of the Mother's Curse hypothesis. In: Philosophical Transactions of the Royal Society B: Biological Sciences. 2020 ; Vol. 375, No. 1790.

Bibtex

@article{c6d2815a0762432fa6f7a5bcd8af4049,
title = "Sex-specific effects of mitochondrial haplotype on metabolic rate in Drosophila melanogaster support predictions of the Mother's Curse hypothesis",
abstract = "Evolutionary theory proposes that maternal inheritance of mitochondria will facilitate the accumulation of mitochondrial DNA (mtDNA) mutations that are harmful to males but benign or beneficial to females. Furthermore, mtDNA haplotypes sampled from across a given species distribution are expected to differ in the number and identity of these {\textquoteleft}male-harming{\textquoteright} mutations they accumulate. Consequently, it is predicted that the genetic variation which delineates distinct mtDNA haplotypes of a given species should confer larger phenotypic effects on males than females (reflecting mtDNA mutations that are male-harming, but female-benign), or sexually antagonistic effects (reflecting mutations that are male-harming, but female-benefitting). These predictions have received support from recent work examining mitochondrial haplotypic effects on adult life-history traits in Drosophila melanogaster. Here, we explore whether similar signatures of male-bias or sexual antagonism extend to a key physiological trait—metabolic rate. We measured the effects of mitochondrial haplotypes on the amount of carbon dioxide produced by individual flies, controlling for mass and activity, across 13 strains of D. melanogaster that differed only in their mtDNA haplotype. The effects of mtDNA haplotype on metabolic rate were larger in males than females. Furthermore, we observed a negative intersexual correlation across the haplotypes for metabolic rate. Finally, we uncovered a male-specific negative correlation, across haplotypes, between metabolic rate and longevity. These results are consistent with the hypothesis that maternal mitochondrial inheritance has led to the accumulation of a sex-specific genetic load within the mitochondrial genome, which affects metabolic rate and that may have consequences for the evolution of sex differences in life history.",
keywords = "mitochondrial DNA, pleiotropy, rate of living, sex specific selective sieve, sexual conflict, sexually antagonistic selection",
author = "Venkatesh Nagarajan-Radha and Ian Aitkenhead and David Clancy and Chown, {Steven L.} and Dowling, {Damian K}",
year = "2020",
month = jan,
day = "30",
doi = "10.1098/rstb.2019.0178",
language = "English",
volume = "375",
journal = "Philosophical Transactions of the Royal Society B: Biological Sciences",
issn = "0962-8436",
publisher = "Royal Society",
number = "1790",

}

RIS

TY - JOUR

T1 - Sex-specific effects of mitochondrial haplotype on metabolic rate in Drosophila melanogaster support predictions of the Mother's Curse hypothesis

AU - Nagarajan-Radha, Venkatesh

AU - Aitkenhead, Ian

AU - Clancy, David

AU - Chown, Steven L.

AU - Dowling, Damian K

PY - 2020/1/30

Y1 - 2020/1/30

N2 - Evolutionary theory proposes that maternal inheritance of mitochondria will facilitate the accumulation of mitochondrial DNA (mtDNA) mutations that are harmful to males but benign or beneficial to females. Furthermore, mtDNA haplotypes sampled from across a given species distribution are expected to differ in the number and identity of these ‘male-harming’ mutations they accumulate. Consequently, it is predicted that the genetic variation which delineates distinct mtDNA haplotypes of a given species should confer larger phenotypic effects on males than females (reflecting mtDNA mutations that are male-harming, but female-benign), or sexually antagonistic effects (reflecting mutations that are male-harming, but female-benefitting). These predictions have received support from recent work examining mitochondrial haplotypic effects on adult life-history traits in Drosophila melanogaster. Here, we explore whether similar signatures of male-bias or sexual antagonism extend to a key physiological trait—metabolic rate. We measured the effects of mitochondrial haplotypes on the amount of carbon dioxide produced by individual flies, controlling for mass and activity, across 13 strains of D. melanogaster that differed only in their mtDNA haplotype. The effects of mtDNA haplotype on metabolic rate were larger in males than females. Furthermore, we observed a negative intersexual correlation across the haplotypes for metabolic rate. Finally, we uncovered a male-specific negative correlation, across haplotypes, between metabolic rate and longevity. These results are consistent with the hypothesis that maternal mitochondrial inheritance has led to the accumulation of a sex-specific genetic load within the mitochondrial genome, which affects metabolic rate and that may have consequences for the evolution of sex differences in life history.

AB - Evolutionary theory proposes that maternal inheritance of mitochondria will facilitate the accumulation of mitochondrial DNA (mtDNA) mutations that are harmful to males but benign or beneficial to females. Furthermore, mtDNA haplotypes sampled from across a given species distribution are expected to differ in the number and identity of these ‘male-harming’ mutations they accumulate. Consequently, it is predicted that the genetic variation which delineates distinct mtDNA haplotypes of a given species should confer larger phenotypic effects on males than females (reflecting mtDNA mutations that are male-harming, but female-benign), or sexually antagonistic effects (reflecting mutations that are male-harming, but female-benefitting). These predictions have received support from recent work examining mitochondrial haplotypic effects on adult life-history traits in Drosophila melanogaster. Here, we explore whether similar signatures of male-bias or sexual antagonism extend to a key physiological trait—metabolic rate. We measured the effects of mitochondrial haplotypes on the amount of carbon dioxide produced by individual flies, controlling for mass and activity, across 13 strains of D. melanogaster that differed only in their mtDNA haplotype. The effects of mtDNA haplotype on metabolic rate were larger in males than females. Furthermore, we observed a negative intersexual correlation across the haplotypes for metabolic rate. Finally, we uncovered a male-specific negative correlation, across haplotypes, between metabolic rate and longevity. These results are consistent with the hypothesis that maternal mitochondrial inheritance has led to the accumulation of a sex-specific genetic load within the mitochondrial genome, which affects metabolic rate and that may have consequences for the evolution of sex differences in life history.

KW - mitochondrial DNA

KW - pleiotropy

KW - rate of living

KW - sex specific selective sieve

KW - sexual conflict

KW - sexually antagonistic selection

U2 - 10.1098/rstb.2019.0178

DO - 10.1098/rstb.2019.0178

M3 - Journal article

VL - 375

JO - Philosophical Transactions of the Royal Society B: Biological Sciences

JF - Philosophical Transactions of the Royal Society B: Biological Sciences

SN - 0962-8436

IS - 1790

M1 - 20190178

ER -