Experimental Evidence Supports a Sex-Specific Selective Sieve in Mitochondrial Genome Evolution

Innocenti, Paolo; Morrow, Edward H.; Dowling, Damian K.

doi:10.1126/science.1201157

Cited by 246 publications

(350 citation statements)

References 29 publications

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“…Indeed, mitochondria-associated genes were downregulated in strains with the resistant Y chromosome. These observations concur with recent observations that mitochondrial variants differently regulate testis gene expression in D. melanogaster (Innocenti et al, 2011). In one similar but more extreme case, the mitochondrial type of Brownsville introgressed into the w 1118 nuclear background can drastically reduce male fertility (Clancy, 2008).…”

Section: Discussionsupporting

confidence: 80%

Natural variation of the Y chromosome suppresses sex ratio distortion and modulates testis-specific gene expression in Drosophila simulans

Branco¹,

Tao

Hartl

et al. 2013

Heredity

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X-linked sex-ratio distorters that disrupt spermatogenesis can cause a deficiency in functional Y-bearing sperm and a femalebiased sex ratio. Y-linked modifiers that restore a normal sex ratio might be abundant and favored when a X-linked distorter is present. Here we investigated natural variation of Y-linked suppressors of sex-ratio in the Winters systems and the ability of these chromosomes to modulate gene expression in Drosophila simulans. Seventy-eight Y chromosomes of worldwide origin were assayed for their resistance to the X-linked sex-ratio distorter gene Dox. Y chromosome diversity caused males to sire B63% to B98% female progeny. Genome-wide gene expression analysis revealed hundreds of genes differentially expressed between isogenic males with sensitive (high sex ratio) and resistant (low sex ratio) Y chromosomes from the same population. Although the expression of about 75% of all testis-specific genes remained unchanged across Y chromosomes, a subset of post-meiotic genes was upregulated by resistant Y chromosomes. Conversely, a set of accessory gland-specific genes and mitochondrial genes were downregulated in males with resistant Y chromosomes. The D. simulans Y chromosome also modulated gene expression in XXY females in which the Y-linked protein-coding genes are not transcribed. The data suggest that the Y chromosome might exert its regulatory functions through epigenetic mechanisms that do not require the expression of protein-coding genes. The gene network that modulates sex ratio distortion by the Y chromosome is poorly understood, other than that it might include interactions with mitochondria and enriched for genes expressed in post-meiotic stages of spermatogenesis.

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Section: Discussionsupporting

confidence: 80%

Natural variation of the Y chromosome suppresses sex ratio distortion and modulates testis-specific gene expression in Drosophila simulans

Branco¹,

Tao

Hartl

et al. 2013

Heredity

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“…when the genome is carried inside of females). That is, if a mutation arises in the mtDNA sequence that is relatively neutral in its effects on females, this mutation will evade selection and could accumulate within populations, even if the effects of the very same mutation are negative for males (Frank & Hurst 1996, Innocenti et al 2011, Frank 2012, Beekman et al 2014. In theory, mtDNA mutations might even arise that augment female function, but decrease male function.…”

Section: Theory Linking the Mitochondria To Male Fertilitymentioning

confidence: 99%

“…All of the fruit fly examples come from studies of D. melanogaster, and many of these have utilised the same panel of naturally occurring mtDNA haplotypes (Clancy et al 2008, 2011, Innocenti et al 2011, Yee et al 2013, Dowling et al 2015, Wolff et al 2016a,b, 2017, which were originally sourced from different global localities and which exhibit generally low levels of sequence divergence (~0.4%); a level of divergence paralleling that seen between major human mtDNA haplogroups (Morrow et al 2015). Replicate genetic strains have been created for each of these haplotypes, with each haplotype placed alongside a standardised isogenic background (i.e.…”

Section: Fruit Fly Case Studiesmentioning

confidence: 99%

Maternal inheritance of mitochondria: implications for male fertility?

Vaught

Dowling

2018

Reproduction

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Evolutionary theory predicts maternal inheritance of the mitochondria will lead to the accumulation of mutations in the mitochondrial DNA (mtDNA) that impair male fertility, but leave females unaffected. The hypothesis has been referred to as 'Mother's Curse'. There are many examples of mtDNA mutations or haplotypes, in humans and other metazoans, associated with decreases in sperm performance, but seemingly few reports of associations involving female reproductive traits; an observation that has been used to support the Mother's Curse hypothesis. However, it is unclear whether apparent signatures of male bias in mitochondrial genetic effects on fertility reflect an underlying biological bias or a technical bias resulting from a lack of studies to have screened for female effects. Here, we conduct a systematic literature search of studies reporting mitochondrial genetic effects on fertility-related traits in gonochoristic metazoans (animals with two distinct sexes). Studies of female reproductive outcomes were sparse, reflecting a large technical sex bias across the literature. We were only able to make a valid assessment of sex specificity of mitochondrial genetic effects in 30% of cases. However, in most of these cases, the effects were male biased, including examples of male bias associated with mtDNA mutations in humans. These results are therefore consistent with the hypothesis that maternal inheritance has enriched mtDNA sequences with mutations that specifically impair male fertility. However, future research that redresses the technical imbalance in studies conducted per sex will be key to enabling researchers to fully assess the wider implications of the Mother's Curse hypothesis to male reproductive biology.Reproduction (2018) 155 R159-R168

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“…Because males do not transmit their mitochondria to offspring, mutations in the mitochondrial genome that are either beneficial or detrimental to males cannot respond directly to selection ( [1][2][3], but see [4]). The importance of this male/female asymmetry in evolutionary response depends critically on the extent to which mitochondrial mutations exert antagonistic effects on male and female fitness [1,5,6].…”

Section: Introductionmentioning

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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Experimental Evidence Supports a Sex-Specific Selective Sieve in Mitochondrial Genome Evolution

Cited by 246 publications

References 29 publications

Natural variation of the Y chromosome suppresses sex ratio distortion and modulates testis-specific gene expression in Drosophila simulans

Natural variation of the Y chromosome suppresses sex ratio distortion and modulates testis-specific gene expression in Drosophila simulans

Maternal inheritance of mitochondria: implications for male fertility?

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

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