Mitochondrial genetic effects on reproductive success: signatures of positive intrasexual, but negative intersexual pleiotropy

Abstract

Theory predicts that maternal inheritance of mitochondria will facilitate the accumulation of mtDNA mutations that are male biased, or even sexually antagonistic, in effect. While there are many reported cases of mtDNA mutations conferring cytoplasmic male sterility in plants, historically it was assumed such mutations would not persist in the streamlined mitochondrial genomes of bilaterian metazoans. Intriguingly, recent cases of mitochondrial variants exerting male biases in effect have come to light in bilaterians. These cases aside, it remains unknown whether the mitochondrial genetic variation affecting phenotypic expression, and in particular reproductive performance, in bilaterians is routinely composed of sex-biased or sex-specific variation. If selection consistently favours mtDNA variants that augment female fitness, but at cost to males, this could shape patterns of pleiotropy and lead to negative intersexual correlations across mtDNA haplotypes. Here, we show that genetic variation across naturally occurring mitochondrial haplotypes affects components of reproductive success in both sexes, in the fruit fly We find that intrasexual correlations across mitochondrial haplotypes, for components of reproductive success, are generally positive, while intersexual correlations are negative. These results accord with theoretical predictions, suggesting that maternal inheritance has led to the fixation of numerous mutations of sexually antagonistic effect.

Sex-specific effects of mitochondrial haplotype on metabolic rate inDrosophila melanogastersupport predictions of the Mother's Curse hypothesis

“…We tested whether 151 signatures of mitochondrial genetic variation were consistent with predictions of the weak 152 (male-biases in size of effect across haplotypes) or strong (negative intersexual correlation 153 across haplotypes) forms of the Mother's Curse hypothesis. We then leveraged trait means for 154 longevity from Camus et al, (2012) and reproductive fitness from Camus and Dowling (2018) 155 of each sex-by-haplotype combination, to test whether mitochondrial variation for metabolic 156 rate is involved in sex-specific trade-offs between physiology and life history phenotypes. To statistically partition mitochondrial haplotype effects from those of the nuclear 161 genetic background, it is necessary to place a set of mtDNA haplotypes alongside a 162 standardized (controlled) nuclear background.…”

Phenotypic variation in mitochondrial function across New Zealand snail populations

“…This latter phenomenon is predicted to result in the accumulation 376 of mutations that are neutral or beneficial in females but deleterious in males 100 . The lack of 377 widespread evidence for mitochondrial mutations with sex-specific fitness effects (but 378 see 35,101,102 ) may point to mechanisms that prevent the spread of male-specific deleterious 379 mutations in mitochondrial genomes (e.g., paternal leakage 103 , inbreeding 104 , kin selection 104 , 380 and/or nuclear-encoded restorers of male function 42,105 ). Asexually produced males, as are 381 occasionally produced in P. antipodarum 60 , represent worst-case scenarios for male-specific 382 mitochondrial performance because their nuclear and mitochondrial genomes have been 383 "trapped" in females for generations but are now being expressed in a male context.…”

“…The biology of these coevolving "mito-nuclear" interactions has been the subject of intense 46 study 16,[35][36][37][38][39][40][41] , but the consequences of coevolution between genomes for function and fitness have 47 only been evaluated in a handful of species and for a handful of mito-nuclear genotypes 16,42-45 . 48 This research has nevertheless yielded critical insights into how mito-nuclear genotypic variation 49 produces phenotypic variation, and demonstrating that mito-nuclear epistasis can be a powerful 50 force for shaping genetic variation in nature 46 .…”

Selfish genes and sexual selection: the impact of genomic parasites on host reproduction

“…However, selfish mitochondria can also generate antagonistic selection by favouring the female function at a cost to male fitness. One such example is a mutation in the cytochrome B identified in D. melanogaster that increase female fitness whilst simultaneously decreasing male fertility (Camus & Dowling, 2018). It is therefore likely that selfish mitochondria also represent a ubiquitous source generating sexually antagonistic selection.…”