Abstract

While numerous studies have demonstrated that mitochondrial genetic variation can shape organismal phenotype, the level of contribution the mitochondrial genotype makes to life‐history phenotype across the life course remains unknown. Furthermore, a clear technical bias has emerged in studies of mitochondrial effects on reproduction, with many studies conducted on males, but few on females. Here, we apply a classic prediction of the evolutionary theory of aging to the mitochondrial genome, predicting the declining force of natural selection with age will have facilitated the accumulation of mtDNA mutations that confer late‐life effects on female reproductive performance. This should lead to increased levels of mitochondrial genetic variation on reproduction at later‐life stages. We tested this hypothesis using thirteen strains of Drosophila melanogaster that each possessed a different mitochondrial haplotype in an otherwise standard nuclear genetic background. We measured fecundity and egg‐to‐adult viability of females over five different age classes ranging from early to late life and quantified the survival of females throughout this time period. We found no significant variation across mitochondrial haplotypes for the reproductive traits, and no mitochondrial effect on the slope of decline in these traits with increasing age. However, we observed that flies that died earlier in the experiment experienced steeper declines in the reproductive traits prior to death, and we also identified maternal and grandparental age effects on the measured traits. These results suggest the mitochondrial variation does not make a key contribution to shaping the reproductive performance of females.

Highlights

  • Sequence variation in mitochondrial DNA is a pervasive characteristic across eukaryotes, but the functional and evolutionary significance of much of this variation remains unclear (Dobler, Rogell, Budar, & Dowling, 2014; Dowling, Friberg, & Lindell, 2008; Galtier, Nabholz, Glémin, & Hurst, 2009)

  • The mitochondrial theory of aging predicts that somatic mutations will accumulate within mitochondrial DNA (mtDNA) sequences with advancing age, causing cellular dysfunction that leads to symptoms of senescence (Balaban, Nemoto, & Finkel, 2005; Dowling & Simmons, 2009; Harman, 1972)

  • The mutation accumulation theory of aging predicts that the genome will be enriched for heritable mutations in the germline that confer later-­life effects, given that the force of natural selection decreases with increasing age following the peak of reproductive productivity (Charlesworth, 2001; Medawar, 1952; Reynolds et al, 2007)

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Summary

| INTRODUCTION

Sequence variation in mitochondrial DNA (mtDNA) is a pervasive characteristic across eukaryotes, but the functional and evolutionary significance of much of this variation remains unclear (Dobler, Rogell, Budar, & Dowling, 2014; Dowling, Friberg, & Lindell, 2008; Galtier, Nabholz, Glémin, & Hurst, 2009). We assessed fecundity, offspring egg-­to-­adult viability, and survival in female flies, each harboring one of 13 different mtDNA haplotypes in an isogenic nuclear background, at each of five distinct age classes, which allowed us to test for the role of mtDNA variation in the expression of these traits across the life course This experimental design explicitly enabled us to test for signatures of mutation accumulation in the mitochondrial genome, consistent with the predictions of the evolutionary theory of aging. | 10724 of mitochondrial variation for fecundity and egg-­to-­adult viability should increase in later age classes

| MATERIALS AND METHODS
| EXPERIMENTAL PROCEDURE
Findings
| DISCUSSION
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