The “unguarded-X” and the genetic architecture of lifespan: Inbreeding results in a potentially maladaptive sex-specific reduction of female lifespan in<i>Drosophila melanogaster</i>

Sultanova, Zahida; Andic, Muhammed; Carazo, Pau

doi:10.1111/evo.13426

Cited by 18 publications

(34 citation statements)

References 64 publications

(147 reference statements)

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“…Despite its long history and intuitive appeal, our results suggest that the UXh may in fact not be a fundamental driver of sex-specific mortality. Since it was first formulated, more than three decades ago, support for the UXh has been scant and indirect [1, 9, 10, 12] and, while this may be due to the inherent difficulties in testing this hypothesis, there are also frequently overlooked reasons to doubt it plays a major role in explaining sex-specific lifespans. For example, the fact that there is likely to be strong selection against big effect X-linked recessive mutations in nature [22], meaning that any mutations that do accumulate on the recombining chromosome should have relatively minor effects.…”

Section: Discussionmentioning

confidence: 99%

“…A recent study further shows that the heterogametic sex tends to exhibit higher mean/maximum lifespan across a wide taxonomic range, but phylogenetic signal and sexual selection could contribute to explain this relationship [10]. In addition, recent experimental evidence shows that “unguarding” the X chromosome in females erases the sex gap in lifespan in Drosophila melanogaster [11, 12] but see [13]. A second hypothesis focuses on the role of the heteromorphic Y (or W) chromosome.…”

Section: Mainmentioning

confidence: 99%

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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%

Section: Mainmentioning

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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“…However, it is difficult to imagine how these effects could mediate female-specific responses in reproductive aging when condition is altered, especially here where we controlled for maternal effects. No support for the unguarded-X hypothesis was found in the most direct test of this hypothesis yet (Brengdahl et al 2018a), but more indirect tests have found patterns consistent with this possibility (Pipoly et al 2015;Carazo et al 2016;Sultanova et al 2018). In any case, it also seems difficult to construct a scenario where X-linked recessive mutations could cause a response in female but not male reproductive aging when condition is altered.…”

Section: Genetic Quality and Sex-specific Aging 767mentioning

confidence: 98%

Genetic Quality Affects the Rate of Male and Female Reproductive Aging Differently in Drosophila melanogaster

Brengdahl¹,

Kimber²,

Maguire-Baxter³

et al. 2018

The American Naturalist

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Dryad data: https://dx.doi.org/10.5061/dryad.5089j74.abstract: Males and females often maximize fitness by pursuing different reproductive strategies, with males commonly assumed to benefit more from increased resource allocation into current reproduction. Such investment should trade off with somatic maintenance and may explain why males frequently live shorter than females. It also predicts that males should experience faster reproductive aging. Here we investigate whether reproductive aging and life span respond to condition differently in male and female Drosophila melanogaster, as predicted if sexual selection has shaped male and female resourceallocation patterns. We manipulate condition through genetic quality by comparing individuals inbred or outbred for a major autosome. While genetic quality had a similar effect on condition in both sexes, condition had a much larger general effect on male reproductive output than on female reproductive output, as expected when sexual selection on vigor acts more strongly on males. We find no differences in reproductive aging between the sexes in low condition, but in high condition reproductive aging is relatively faster in males. No corresponding sex-specific change was found for life span. The sex difference in reproductive aging appearing in high condition was specifically due to a decreased aging rate in females rather than any change in males. Our results suggest that females age slower than males in high condition primarily because sexual selection has favored sex differences in resource allocation under high condition, with females allocating relatively more toward somatic maintenance than males.

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“…Families that are exclusively self-compatible have lower net diversification rates than those that are predominantly self-incompatible (Ferrer and Good, 2012). Ostensibly selfing species having higher extinction rates than outcrossers (Wright et al, 2013) in part due to a reduced ability to adapt, especially to new environments (Hartfield et al, 2017).…”

Section: Why Wgd Are Not Followed By Immediate Diversification Thrustsmentioning

confidence: 99%

Has the Polyploid Wave Ebbed?

Levin

2020

Front. Plant Sci.

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There was a wave of whole genome duplications (WGD) during and subsequent to the K-Pg interface, which was followed by an increase in the proportion of species that were polyploid. I consider why this wave of polyploid speciation has continued to rise through the divergent evolution of polyploid lineages, and through rounds of homoploid and heteroploid chromosomal change. I also consider why the polyploid speciation wave is likely to rise in the next millennium. I propose that the speed of polyploid genesis through ploidal increase and through diversification among polyploids likely will be greater than the speed of diploid speciation. The increase in polyploid diversity is expected to lag well behind episodes of WGD, owing to the very long period required for species diversification either by lineage splitting or additional rounds of polyploidy, in addition to the long period of genomic adjustment to higher ploidal levels in neopolyploids.

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The “unguarded-X” and the genetic architecture of lifespan: Inbreeding results in a potentially maladaptive sex-specific reduction of female lifespan inDrosophila melanogaster

Cited by 18 publications

References 64 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

Genetic Quality Affects the Rate of Male and Female Reproductive Aging Differently in Drosophila melanogaster

Has the Polyploid Wave Ebbed?

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