Mother's curse: the effect of mtDNA on individual fitness and population viability

Gemmell, Neil J.; Metcalf, Victoria J.; Allendorf, Fred W.

doi:10.1016/j.tree.2004.02.002

Cited by 325 publications

(385 citation statements)

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“…Maternal inheritance of mitochondria creates male/female asymmetries in response to selection that have potentially important implications for evolutionary processes ranging from sexual differences in longevity and disease susceptibility to population viability and speciation [13,54]. Paradoxically, in the field of sexual selection, where maternal inheritance of mitochondria may well have its greatest impact, female-limited response to selection remains inadequately investigated.…”

Section: Discussionmentioning

confidence: 99%

Sisters' curse: sexually antagonistic effects constrain the spread of a mitochondrial haplogroup superior in sperm competition

et al. 2014

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Maternal inheritance of mitochondria creates a sex-specific selective sieve with implications for male longevity, disease susceptibility and infertility. Because males are an evolutionary dead end for mitochondria, mitochondrial mutations that are harmful or beneficial to males but not females cannot respond directly to selection. Although the importance of this male/female asymmetry in evolutionary response depends on the extent to which mitochondrial mutations exert antagonistic effects on male and female fitness, few studies have documented sex-specific selection acting on mitochondria. Here, we exploited the discovery of two highly divergent mitochondrial haplogroups (A and B2) in central Panamanian populations of the pseudoscorpion Cordylochernes scorpioides. Next-generation sequencing and phylogenetic analyses suggest that selection on the ND4 and ND4L mitochondrial genes may partially explain sexually antagonistic mitochondrial effects on reproduction. Males carrying the rare B2 mitochondrial haplogroup enjoy a marked advantage in sperm competition, but B2 females are significantly less sexually receptive at second mating than A females. This reduced propensity for polyandry is likely to significantly reduce female lifetime reproductive success, thereby limiting the spread of the male beneficial B2 haplogroup. Our findings suggest that maternal inheritance of mitochondria and sexually antagonistic selection can constrain male adaptation and sexual selection in nature.

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Section: Discussionmentioning

confidence: 99%

Sisters' curse: sexually antagonistic effects constrain the spread of a mitochondrial haplogroup superior in sperm competition

et al. 2014

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“…biologists in the role of the mitochondrial genome in adaptive evolution, only a limited number of studies has tested the effect of mitochondrial polymorphism on life-history traits and fitness (reviewed in Ballard and Whitlock 2004;Gemmell et al 2004;Rand et al 2004). In fact, variation in mitochondrial genes by tradition has been assumed to be selectively neutral (see Rand 2001;Ballard and Whitlock 2004;Ballard and Rand 2005).…”

Section: Espite An Increasing Interest Among Evolutionarymentioning

confidence: 99%

Intergenomic Epistasis for Fitness: Within-Population Interactions Between Cytoplasmic and Nuclear Genes in Drosophila melanogaster

et al. 2007

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The symbiotic relationship between the mitochondrial and nuclear genomes coordinates metabolic energy production and is fundamental to life among eukaryotes. Consequently, there is potential for strong selection to shape interactions between these two genomes. Substantial research attention has focused on the possibility that within-population sequence polymorphism in mitochondrial DNA (mtDNA) is maintained by mitonuclear fitness interactions. Early theory predicted that selection will often eliminate mitochondrial polymorphisms. However, recent models demonstrate that intergenomic interactions can promote the maintenance of polymorphism, especially if the nuclear genes involved are linked to the X chromosome. Most empirical studies to date that have assessed cytonuclear fitness interactions have studied variation across populations and it is still unclear how general and strong such interactions are within populations. We experimentally tested for cytonuclear interactions within a laboratory population of Drosophila melanogaster using 25 randomly sampled cytoplasmic genomes, expressed in three different haploid nuclear genetic backgrounds, while eliminating confounding effects of intracellular bacteria (e.g., Wolbachia). We found sizable cytonuclear fitness interactions within this population and present limited evidence suggesting that these effects were sex specific. Moreover, the relative fitness of cytonuclear genotypes was environment specific. Sequencing of mtDNA (2752 bp) revealed polymorphism within the population, suggesting that the observed cytoplasmic genetic effects may be mitochondrial in origin.

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“…Genetic variation in the mitochondrial genome has traditionally been considered selectively neutral. Consequently, sequence divergence in mitochondrial DNA (mtDNA) has been used extensively as a tool to infer evolutionary histories, with the assumption that mtDNA evolves solely by accumulating neutral mutations (see Gemmel et al 2004;Ballard and Rand 2005). However, this traditional view of the mitochondrial genome is currently changing.…”

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confidence: 99%

“…Thus, mtDNA is likely to play a role in adaptive evolution. However, our knowledge of its influence on phenotypic variation is still very incomplete (for recent reviews see Rand et al 2004;Ballard and Whitlock 2004;Gemmel et al 2004;Ballard and Rand 2005).Mitochondrial DNA has also been suggested to play an important role in the evolution of aging (Harman 1956;Tanaka et al 1998; de Benedicts et al 2000;Niemi et al 2005; reviewed in Ballard and Whitlock 2004). Products of mtDNA clearly have a profound role in energy metabolism.…”

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Within-Population Variation in Cytoplasmic Genes Affects Female Life Span and Aging in Drosophila Melanogaster

et al. 2006

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Abstract. It has been suggested that mitochondrial DNA (mtDNA) may play an important role in aging. Yet, few empirical studies have tested this hypothesis, partly because the degree of sequence polymorphism in mtDNA is assumed to be low. However, low sequence variation may not necessarily translate into low phenotypic variation. Here, we report an experiment that tests whether there is within-population variation in cytoplasmic genes for female longevity and senescence. To achieve this, we randomly selected 25 ''mitochondrial founders'' from a single, panmictic population of Drosophila melanogaster and used these founders to generate distinct ''mt'' lines in which we controlled for the nuclear background by successive backcrossing. Potential confounding effects of cytoplasmically transmitted bacteria were eliminated by tetracycline treatment. The mt lines were then assayed for differences in longevity, Gompertz intercept (frailty), and demographic rate of change in mortality with age (rate-of-senescence) in females. We found significant cytoplasmic effects on all three variables. This provides evidence that genetic variation in cytoplasmic genes, presumably mtDNA, contributes to variation in female mortality and aging. Genetic variation in the mitochondrial genome has traditionally been considered selectively neutral. Consequently, sequence divergence in mitochondrial DNA (mtDNA) has been used extensively as a tool to infer evolutionary histories, with the assumption that mtDNA evolves solely by accumulating neutral mutations (see Gemmel et al. 2004;Ballard and Rand 2005). However, this traditional view of the mitochondrial genome is currently changing. In fact, non-neutral evolution of mtDNA has now been implied in several recent studies demonstrating that specific cytoplasmic gene products exhibit reduced or altered function when coexpressed in nuclear genomes derived from different populations (reviewed in Rand 2001;Rand et al. 2004;Ballard and Rand 2005). Thus, mtDNA is likely to play a role in adaptive evolution. However, our knowledge of its influence on phenotypic variation is still very incomplete (for recent reviews see Rand et al. 2004;Ballard and Whitlock 2004;Gemmel et al. 2004;Ballard and Rand 2005).Mitochondrial DNA has also been suggested to play an important role in the evolution of aging (Harman 1956;Tanaka et al. 1998; de Benedicts et al. 2000;Niemi et al. 2005; reviewed in Ballard and Whitlock 2004). Products of mtDNA clearly have a profound role in energy metabolism. Because variation in metabolic rate may be associated with variation in life span (e.g., Sacher 1977), genetic variation in mtDNA could conceivably affect both metabolism and aging (Beckman and Ames 1998; Speakman 2005). Currently, empirical evidence for an association between metabolic rate and aging is limited (Brand 2000;Speakman et al. 2004). Khazaeli et al. (2005) found no relationship between metabolic rate and survival in Drosophila melanogaster lines artificially selected for increased life span. However, the results of ...

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Mother's curse: the effect of mtDNA on individual fitness and population viability

Cited by 325 publications

References 49 publications

Sisters' curse: sexually antagonistic effects constrain the spread of a mitochondrial haplogroup superior in sperm competition

Sisters' curse: sexually antagonistic effects constrain the spread of a mitochondrial haplogroup superior in sperm competition

Intergenomic Epistasis for Fitness: Within-Population Interactions Between Cytoplasmic and Nuclear Genes in Drosophila melanogaster

Within-Population Variation in Cytoplasmic Genes Affects Female Life Span and Aging in Drosophila Melanogaster

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