Faraway, so close. The comparative method and the potential of non-model animals in mitochondrial research

Milani, Liliana; Ghiselli, Fabrizio

doi:10.1098/rstb.2019.0186

Cited by 11 publications

(7 citation statements)

References 131 publications

(181 reference statements)

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“…We examined this relationship in two different nutritional environments: standard rearing food and a high-protein food. G × E in Drosophila [24,45,46] and highlight the difficulty of generalizing about mitonuclear effects without considering a wide sample of mitonuclear variation across populations [47,48]. While nuclear genes largely shape life-history traits in response to diet, mitonuclear interactions modulate these nuclear effects in ways that are not easy to predict.…”

Section: Discussionmentioning

confidence: 99%

Impact of mitonuclear interactions on life-history responses to diet

Camus

O'Leary

Reuter

et al. 2019

Phil. Trans. R. Soc. B

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Mitochondria are central to both energy metabolism and biosynthesis. Mitochondrial function could therefore influence resource allocation. Critically, mitochondrial function depends on interactions between proteins encoded by the mitochondrial and nuclear genomes. Severe incompatibilities between these genomes can have pervasive effects on both fitness and longevity. How milder deficits in mitochondrial function affect life-history trade-offs is less well understood. Here, we analyse how mitonuclear interactions affect the trade-off between fecundity and longevity in Drosophila melanogaster . We consider a panel of 10 different mitochondrial DNA haplotypes against two contrasting nuclear backgrounds ( w 1118 (WE) and Zim53 (ZIM)) in response to high-protein versus standard diet. We report strikingly different responses between the two nuclear backgrounds. WE females have higher fecundity and decreased longevity on high protein. ZIM females have much greater fecundity and shorter lifespan than WE flies on standard diet. High protein doubled their fecundity with no effect on longevity. Mitochondrial haplotype reflected nuclear life-history trade-offs, with a negative correlation between longevity and fecundity in WE flies and no correlation in ZIM flies. Mitonuclear interactions had substantial effects but did not reflect genetic distance between mitochondrial haplotypes. We conclude that mitonuclear interactions can have significant impact on life-history trade-offs, but their effects are not predictable by relatedness. This article is part of the theme issue ‘Linking the mitochondrial genotype to phenotype: a complex endeavour’.

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Section: Discussionmentioning

confidence: 99%

Impact of mitonuclear interactions on life-history responses to diet

Camus

O'Leary

Reuter

et al. 2019

Phil. Trans. R. Soc. B

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“…The opportunity for natural selection to act directly on sperm mitochondria makes the DUI system an attractive model to evaluate the phenotype resulting from a male-specific evolution of mitochondria and thus the adaptive value of paternally inherited mtDNA variants [27]. Furthermore, comparing the functions of male gametes carrying either male-or femalederived mitochondria (DUI versus SMI) brings an exceptional opportunity to test the effectiveness of the mother's curse hypothesis in bivalves.…”

Section: Introductionmentioning

confidence: 99%

Linking paternally inherited mtDNA variants and sperm performance

Bettinazzi

Nadarajah

Dalpé

et al. 2019

Phil. Trans. R. Soc. B

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Providing robust links between mitochondrial genotype and phenotype is of major importance given that mitochondrial DNA (mtDNA) variants can affect reproductive success. Because of the strict maternal inheritance (SMI) of mitochondria in animals, haplotypes that negatively affect male fertility can become fixed in populations. This phenomenon is known as ‘mother's curse’. Doubly uniparental inheritance (DUI) of mitochondria is a stable exception in bivalves, which entails two mtDNA lineages that evolve independently and are transmitted separately through oocytes and sperm. This makes the DUI mitochondrial lineages subject to different sex-specific selective sieves during mtDNA evolution, thus DUI is a unique model to evaluate how direct selection on sperm mitochondria could contribute to male reproductive fitness. In this study, we tested the impact of mtDNA variants on sperm performance and bioenergetics in DUI and SMI species. Analyses also involved measures of sperm performance following inhibition of main energy pathways and sperm response to oocyte presence. Compared to SMI, DUI sperm exhibited (i) low speed and linearity, (ii) a strict OXPHOS-dependent strategy of energy production, and (iii) a partial metabolic shift towards fermentation following egg detection. Discussion embraces the adaptive value of mtDNA variation and suggests a link between male-energetic adaptation, fertilization success and paternal mitochondria preservation. This article is part of the theme issue ‘Linking the mitochondrial genotype to phenotype: a complex endeavour’.

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“…2019 ; 2020 ). As such, the DUI system represents a unique model to test how variation in sequence (heteroplasmy) can vary within and between distinct sex-linked haplotypes, tissues, and individuals, providing insight on how selection shapes the landscape of mtDNA heterogeneity and mt evolution ( Milani and Ghiselli 2020 ).…”

Section: Introductionmentioning

confidence: 99%

A Naturally Heteroplasmic Clam Provides Clues about the Effects of Genetic Bottleneck on Paternal mtDNA

Iannello

Bettinazzi

Breton

et al. 2021

Genome Biology and Evolution

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Mitochondrial DNA (mtDNA) is present in multiple copies within an organism. Since these copies are not identical, a single individual carries a heterogeneous population of mtDNAs, a condition known as heteroplasmy. Several factors play a role in the dynamics of the within-organism mtDNA population: among them genetic bottlenecks, selection, and strictly maternal inheritance are known to shape the levels of heteroplasmy across mtDNAs. In Metazoa, the only evolutionarily stable exception to the strictly maternal inheritance of mitochondria is the doubly uniparental inheritance (DUI), reported in 100+ bivalve species. In DUI species there are two highly divergent mtDNA lineages, one inherited through oocyte mitochondria (F-type) and the other through sperm mitochondria (M-type). Having both parents contributing to the mtDNA pool of the progeny makes DUI a unique system to study the dynamics of mtDNA populations. Since in bivalves the spermatozoon has few mitochondria (4-5), M-type mtDNA faces a tight bottleneck during embryo segregation, one of the narrowest mitochondrial bottlenecks investigated so far. Here, we analyzed the F- and M-type mtDNA variability within individuals of the DUI species Ruditapes philippinarum, and we investigated for the first time the effects of such a narrow bottleneck affecting mtDNA populations. As a potential consequence of this narrow bottleneck, the M-type mtDNA shows a large variability in different tissues, a condition so pronounced that it leads to genotypes from different tissues of the same individual not to cluster together. We believe such results may help understanding the effect of low population size on mtDNA bottleneck.

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Faraway, so close. The comparative method and the potential of non-model animals in mitochondrial research

Cited by 11 publications

References 131 publications

Impact of mitonuclear interactions on life-history responses to diet

Impact of mitonuclear interactions on life-history responses to diet

Linking paternally inherited mtDNA variants and sperm performance

A Naturally Heteroplasmic Clam Provides Clues about the Effects of Genetic Bottleneck on Paternal mtDNA

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