Article

Age specificity of inbreeding load in Drosophila melanogaster and implications for the evolution of late-life mortality plateaus.

Program in Ecology and Evolutionary Biology, University of Illinois, Urbana-Champaign, Illinois 61801, USA.
Genetics (Impact Factor: 4.87). 10/2007; 177(1):587-95. DOI: 10.1534/genetics.106.070078
Source: PubMed

ABSTRACT Current evolutionary theories explain the origin of aging as a byproduct of the decline in the force of natural selection with age. These theories seem inconsistent with the well-documented occurrence of late-life mortality plateaus, since under traditional evolutionary models mortality rates should increase monotonically after sexual maturity. However, the equilibrium frequencies of deleterious alleles affecting late life are lower than predicted under traditional models, and thus evolutionary models can accommodate mortality plateaus if deleterious alleles are allowed to have effects spanning a range of neighboring age classes. Here we test the degree of age specificity of segregating alleles affecting fitness in Drosophila melanogaster. We assessed age specificity by measuring the homozygous fitness effects of segregating alleles across the adult life span and calculated genetic correlations of these effects across age classes. For both males and females, we found that allelic effects are age specific with effects extending over 1-2 weeks across all age classes, consistent with modified mutation-accumulation theory. These results indicate that a modified mutation-accumulation theory can both explain the origin of senescence and predict late-life mortality plateaus.

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Available from: Kimberly A Hughes, Mar 14, 2014
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    ABSTRACT: In principle, parental relatedness, parental age, and the age of parental gametes can all influence offspring fitness through inbreeding depression and the parental effects of organismal and postmeiotic gametic senescence. However, little is known about the extent to which these factors interact and contribute to fitness variation. Here, we show that, in Drosophila melanogaster, offspring viability is strongly affected by a three-way interaction between parental relatedness, parental age, and gametic age at successive developmental stages. Overall egg-to-adult viability was lowest for offspring produced with old gametes of related, young parents. This overall effect was largely determined at the pupa-adult stage, although three-way interactions between parental relatedness, parental age and gametic age also explained variation in egg hatchability and larva-pupa survival. Controlling for the influence of parental and gametic age, we show that inbreeding depression is negligible for egg hatchability but significant at the larva-pupa and pupa-adult stages. At the pupa-adult stage, where offspring could be sexed, parental relatedness, parental age, and gametic age interacted differently in male and female offspring, with daughters suffering higher inbreeding depression than sons. Collectively, our results demonstrate that the architecture of offspring fitness is strongly influenced by a complex interaction between parental effects, inbreeding depression and offspring sex.
    Evolution 10/2013; 67(10):3043-3051. DOI:10.1111/evo.12131 · 4.66 Impact Factor
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    ABSTRACT: In principle, parental relatedness, parental age, and the age of parental gametes can all influence offspring fitness through inbreeding depression and the parental effects of organismal and postmeiotic gametic senescence. However, little is known about the extent to which these factors interact and contribute to fitness variation. Here, we show that, in Drosophila melanogaster, offspring viability is strongly affected by a three-way interaction between parental relatedness, parental age, and gametic age at successive developmental stages. Overall egg-to-adult viability was lowest for offspring produced with old gametes of related, young parents. This overall effect was largely determined at the pupa–adult stage, although three-way interactions between parental relatedness, parental age and gametic age also explained variation in egg hatchability and larva-pupa survival. Controlling for the influence of parental and gametic age, we show that inbreeding depression is negligible for egg hatchability but significant at the larva–pupa and pupa–adult stages. At the pupa–adult stage, where offspring could be sexed, parental relatedness, parental age, and gametic age interacted differently in male and female offspring, with daughters suffering higher inbreeding depression than sons. Collectively, our results demonstrate that the architecture of offspring fitness is strongly influenced by a complex interaction between parental effects, inbreeding depression and offspring sex. K E Y W O R D S : Inbreeding depression, ontogenesis, parental effects, senescence, unguarded X-hypothesis. Inbreeding, the mating of related individuals, can depress off-spring fitness through the expression of deleterious recessive alleles and loss of heterozygous advantage (Charlesworth and Charlesworth 1987). Recent work has identified inbreeding de-pression as a fundamental determinant of the dynamics (Keller and Waller 2002; Grady et al. 2006; Walling et al. 2011) and evolu-tion of natural populations (Andersson 2012; Dierkes et al. 2012). The magnitude of inbreeding depression varies with environmen-tal conditions (Armbruster and Reed 2005; Fox and Reed 2011), genetic architecture (Fox et al. 2006), and life-history stages (Charlesworth and Hughes 1996). For example, Charlesworth and Hughes (1996) demonstrated that inbred male fruit flies, Drosophila melanogaster, suffer increasing fitness costs as they age, indicating that effects of inbreeding depression can be age de-pendent. This could be due to the accumulation of late-acting dele-terious mutations that are age specific (Charlesworth and Hughes 1996; Reynolds et al. 2007). It is similarly likely that mechanisms of parental senescence might also act as important modulators of the magnitude of inbreeding depression in the offspring, however this hypothesis has received surprisingly little consideration. Senescence can occur at two distinct levels. At the organis-mal level, senescence refers to a decline in survival and reproduc-tive ability with advancing age (Rose 1991; Finch and Kirkwood 2000) due to mutation accumulation or antagonistic pleiotropy