Quantitative genetic tests of recent senescence theory: age-specific mortality and male fertility in Drosophila melanogaster

Abstract

Quantitative genetic models of aging predict that additive genetic variance for fitness components should increase with age. However, recent studies have found that at very late ages, the genetic variance components decline. This decline may be due to an age-related drop in reproductive effort. If genetic variance in reproductive effort affects the genetic variance in mortality, the decline in reproductive effort at late ages should lead to a decrease in the genetic variance in mortality. To test this, we carried out a large-scale quantitative genetic analysis of age-specific mortality and fertility in virgin male Drosophila melanogaster. As in earlier studies, we found that the additive variance for age-specific mortality and fertility declined at late ages. Also, recent theoretical developments provide new predictions to distinguish between the mutation accumulation (MA) and antagonistic pleiotropy (AP) models of senescence. The deleterious effects of inbreeding are expected to increase with age under MA, but not under AP. This prediction was supported for both age-specific mortality and male fertility. Under AP, the ratio of dominance to additive variance is expected to decline with age. This predicition, too, was supported by the data analyzed here. Taken together, these analyses provide support for both the models playing a role in the aging process. We argue that the time has come to move beyond a simple comparison of these genetic models, and to think more deeply about the evolutionary causes and consequences of senescence.

Intra-locus sexual conflict and sexually antagonistic genetic variation in hermaphroditic animals

“…The idea of antagonistic pleiotropy was originally developed in the context of senescence [67], and states that alleles that increase fitness at early stages but have deleterious effects late in life will tend to accumulate in the population because selection does not operate as efficiently later on in life. Antagonistic pleiotropy has some empirical support in the context of senescence [68,69], and its role in senescence has in fact recently been investigated in a hermaphroditic species [70]. It seems reasonable that sexual antagonism via antagonistic pleiotropy could operate in sequential hermaphrodites, where alleles that increase fitness in the first sex at the expense of the second sex should spread owing to a decreased efficiency of selection at later stages in life.…”

Analysis of the effects of inbreeding on lifespan and starvation resistance in Drosophila melanogaster

“…Since then additional direct and indirect evidence for the deleterious effects of inbreeding on adult survival has been provided by a number of studies on species such as D. melanogaster and D. simulans (e.g. Hughes 1995a; Snoke and Promislow 2003;Vermeulen and Bijlsma 2004;Swindell and Bouzat 2006a;Vermeulen et al 2008;Wright et al 2008).…”

Environmental effects on sex differences in the genetic load for adult lifespan in a seed-feeding beetle

“…Most tests of mutation accumulation models with Drosophila have found that the genetic load and/or genetic variance for fitness traits increase with age (Snoke and Promislow, 2003;Gong et al, 2006;Swindell and Bouzat, 2006;Borash et al, 2007), although results have varied among lines and/or differed between the sexes (Lesser et al, 2006;Reynolds et al, 2007). The evidence is more equivocal in non-Drosophila systems (Wilson et al, 2008).…”

“…For example, as beetles age, the mortality rate decelerates (Fox and Moya-Larañ o, 2003), approaching a mortality plateau that is the same for inbred and outbred beetles (that is, the u(t) curves converge), and the estimated inbreeding load converges on 0. The presence of mortality plateaus, or the age at which populations reach their plateau, may reflect adaptation to the laboratory (Promislow and Tatar, 1998;Snoke and Promislow, 2003;Rauser et al, 2006). However, mortality plateaus have been observed in a variety of experiments with seed beetles, including populations recently collected from the field and not adapted to the laboratory culture (Tatar et al, 1993;Tatar and Carey, 1995;Fox et al, 2003b;Fox and Moya-Larañ o, 2003), that also provide no evidence for an increase in the inbreeding load with age (Fox et al, 2006).…”

“…One method of testing this mutation accumulation hypothesis has been to quantify the inbreeding load (genetic or mutational load) affecting adult lifespan, or other fitness traits, and test whether the inbreeding load changes with age; the mutation accumulation hypothesis predicts that the inbreeding load will increase with age (Charlesworth and Hughes, 1996;Hughes and Reynolds, 2005). Studies of Drosophila using this approach, or comparing the ratio of dominance to additive genetic variance, have generally supported the mutation accumulation hypothesis (Snoke and Promislow, 2003;Swindell and Bouzat, 2006;Reynolds et al, 2007). In contrast, a few recent studies of other model systems have found that the inbreeding load does not always increase with age (Fox et al, 2006;Wilson et al, 2008), and other studies have shown that the relationship between age and the inbreeding load varies between the sexes or among populations/lines (Lesser et al, 2006;Reynolds et al, 2007;Keller et al, 2008).…”