Mother’s curse and indirect genetic effects: Do males matter to mitochondrial genome evolution?

Keaney, Thomas A.; Wong, Heidi W. S.; Dowling, Damian K.; Jones, Therésa M.; Holman, Luke

doi:10.1111/jeb.13561

Cited by 9 publications

(9 citation statements)

References 75 publications

(113 reference statements)

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“…An exciting possibility is that cyto-nuclear interactions may contribute to explain marked “toxic Y” effects in mammals, but not in birds. Given that Y chromosomes are not inherited along with mitochondrial DNA (and other cytoplasmic products), there is less scope for cyto-nuclear co-evolution in males vs. females with X/Y genetic determination systems (but see [26]). This is not the case in males of species with ZW sex-determination systems because in these species females are the heterogametic sex, and hence copies of both sex chromosomes are inherited maternally along with the cytoplasm.…”

Section: Discussionmentioning

confidence: 99%

Genetic sex determination and sex-specific lifespan in tetrapods – evidence of a toxic Y effect

Sultanova

Downing

Carazo

2020

Preprint

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26Sex-specific lifespans are ubiquitous across the tree of life and exhibit broad taxonomic 27 patterns that remain a puzzle, such as males living longer than females in birds and vice versa 28 in mammals. The prevailing "unguarded-X" hypothesis (UXh) explains this by differential 29 expression of recessive mutations in the X/Z chromosome of the heterogametic sex (e.g., 30females in birds and males in mammals), but has only received indirect support to date. An 31 alternative hypothesis is that the accumulation of deleterious mutations and repetitive 32 elements on the Y/W chromosome might lower the survival of the heterogametic sex ("toxic 33 Y" hypothesis). Here, we report lower survival of the heterogametic relative to the 34 homogametic sex across 138 species of birds, mammals, reptiles and amphibians, as expected 35 if sex chromosomes shape sex-specific lifespans. We then analysed bird and mammal 36 karyotypes and found that the relative sizes of the X and Z chromosomes are not associated 37 with sex-specific lifespans, contrary to UXh predictions. In contrast, we found that Y size 38 correlates negatively with male survival in mammals, where toxic Y effects are expected to be 39 particularly strong. This suggests that small Y chromosomes benefit male lifespans. Our 40 results confirm the role of sex chromosomes in explaining sex differences in lifespan, but 41indicate that, at least in mammals, this is better explained by "toxic Y" rather than UXh 42 effects. 43 44 45 46 47 48 MAIN 52Sexual dimorphism in lifespan is widespread across the tree of life, including among tetrapods 53[1]. Which sex lives longer varies considerably in both direction and magnitude. For example, 54 females live three times longer than males in the brown antechinus, a small marsupial, while 55 males are twice as likely as females to survive from one year to the next in Arabian babblers, 56 a passerine bird [2, 3]. In humans, the lifespan gap is estimated to be 4.8 years -female life 57 expectancy is 74.7 years while male life expectancy is 69.9 years [4]. Understanding the 58 dynamic nature of sex differences in lifespan across taxa remains an unsolved problem in 59 evolutionary biology. To date, empirical studies have focused on adaptive hypotheses 60 stemming from sex-specific differences in how natural selection operates on females and 61 males [1, 5-8]. Despite their prominent role in explaining sex differences in ageing, adaptive 62processes seem unable to explain the observation that the homogametic sex tends to live 63 longer than the heterogametic sex across a wide taxonomic range [1, 9]. 64 65There are at least two reasons why sex chromosomes should directly contribute to the 66 evolution of different female and male lifespans [9, 10]. First, the unguarded X hypothesis 67 (UXh) predicts increased mortality of the heterogametic sex due to the expression of 68 deleterious recessive mutations that accumulate in the non-recombining parts of the X (or Z) 69 chromosome [10]. Because these mutations are masked in the homogametic s...

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Section: Discussionmentioning

confidence: 99%

Genetic sex determination and sex-specific lifespan in tetrapods – evidence of a toxic Y effect

Sultanova

Downing

Carazo

2020

Preprint

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“…Sex-biased effects of mitochondrial diversity have been observed in experiments (Dowling & Adrian, 2019;Vaught & Dowling, 2018), but the evidence in natural populations is scarce (Beekman et al, 2014). This could be because mitochondrial mutations in fact respond to selection in males, as population-genetic models predict would happen when there is inbreeding or kin selection (Keaney et al 2019;, or when both parents contribute their mitochondria to the zygote (Kuijper et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

“…This could be because mitochondrial mutations in fact respond to selection in males, as population‐genetic models predict would happen when there is inbreeding or kin selection (Keaney et al. 2019; Wade & Brandvain, 2009), or when both parents contribute their mitochondria to the zygote (Kuijper et al., 2015). Our current results show that both paternal leakage and reduced sex linkage of nuclear genes interacting with mitochondria may evolve to reduce the severity of these predicted male‐harming effects.…”

Section: Discussionmentioning

confidence: 99%

Sexually antagonistic evolution of mitochondrial and nuclear linkage

Radzvilavicius

Layh

Hall

et al. 2021

J of Evolutionary Biology

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Across eukaryotes, genes encoding bioenergetic machinery are located in both mitochondrial and nuclear DNA, and incompatibilities between the two genomes can be devastating. Mitochondria are often inherited maternally, and theory predicts sex‐specific fitness effects of mitochondrial mutational diversity. Yet how evolution acts on linkage patterns between mitochondrial and nuclear genomes is poorly understood. Using novel mito‐nuclear population‐genetic models, we show that the interplay between nuclear and mitochondrial genes maintains mitochondrial haplotype diversity within populations, and selects both for sex‐independent segregation of mitochondrion‐interacting genes and for paternal leakage. These effects of genetic linkage evolution can eliminate male‐harming fitness effects of mtDNA mutational diversity. With maternal mitochondrial inheritance, females maintain a tight mitochondrial–nuclear match, but males accumulate mismatch mutations because of the weak statistical associations between the two genomic components. Sex‐independent segregation of mitochondria‐interacting loci improves the mito‐nuclear match. In a sexually antagonistic evolutionary process, male nuclear alleles evolve to increase the rate of recombination, whereas females evolve to suppress it. Paternal leakage of mitochondria can evolve as an alternative mechanism to improve the mito‐nuclear linkage. Our modelling framework provides an evolutionary explanation for the observed paucity of mitochondrion‐interacting genes on mammalian sex chromosomes and for paternal leakage in protists, plants, fungi and some animals.

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“…Sex-biased effects of mitochondrial diversity have been observed in experiments (Vaught and Dowling, 2018;Dowling and Adrian, 2019), but the evidence in natural populations is scarce (Beekman et al, 2014). This could be because mitochondrial mutations in fact respond to selection in males, as population-genetic models predict would happen when there is inbreeding or kin selection (Wade and Brandvain, 2009;Keaney et al 2019), or when both parents contribute their mitochondria to the zygote (Kuijper et al, 2015). Our current results show that both paternal leakage and reduced sex-linkage of nuclear genes interacting with mitochondria may evolve to reduce the severity of these predicted male-harming effects.…”

Section: Discussionmentioning

confidence: 99%

Sexually antagonistic evolution of mitochondrial and nuclear linkage

Radzvilavicius

Layh

Hall

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

Across eukaryotes, genes encoding bioenergetic machinery are located in both mitochondrial and nuclear DNA, and incompatibilities between the two genomes can be devastating. Mitochondria are often inherited maternally, and theory predicts sex-specific fitness effects of mitochondrial mutational diversity. Yet how evolution acts on linkage patterns between mitochondrial and nuclear genomes is poorly understood. Using novel mito-nuclear population genetic models, we show that the interplay between nuclear and mitochondrial genes maintains mitochondrial haplotype diversity within populations, and it selects both for sex-independent segregation of mitochondrion-interacting genes and for paternal leakage. These effects of genetic linkage evolution can eliminate male-harming fitness effects of mtDNA mutational diversity. With maternal mitochondrial inheritance, females maintain a tight mitochondrial-nuclear match, but males accumulate mismatch mutations because of the weak statistical associations between the two genomic components. Sex-independent segregation of mitochondria-interacting loci improves the mito-nuclear match. In a sexually antagonistic evolutionary process, male nuclear alleles evolve to increase the rate of recombination, while females evolve to suppress it. Paternal leakage of mitochondria can evolve as an alternative mechanism to improve the mito-nuclear linkage. Our modelling framework provides an evolutionary explanation for the observed paucity of mitochondrion-interacting genes on mammalian sex chromosomes and for paternal leakage in protists, plants, fungi, and some animals.

show abstract

Mother’s curse and indirect genetic effects: Do males matter to mitochondrial genome evolution?

Cited by 9 publications

References 75 publications

Genetic sex determination and sex-specific lifespan in tetrapods – evidence of a toxic Y effect

Genetic sex determination and sex-specific lifespan in tetrapods – evidence of a toxic Y effect

Sexually antagonistic evolution of mitochondrial and nuclear linkage

Sexually antagonistic evolution of mitochondrial and nuclear linkage

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