Inbreeding Depression and Male Survivorship in Drosophila: Implications for Senescence Theory

Abstract

The extent to which inbreeding depression affects longevity and patterns of survivorship is an important issue from several research perspectives, including evolutionary biology, conservation biology, and the genetic analysis of quantitative traits. However, few previous inbreeding depression studies have considered longevity as a focal life-history trait. We maintained laboratory populations of Drosophila melanogaster at census population sizes of 2 and 10 male-female pairs for up to 66 generations and performed repeated assays of male survivorship throughout this time period. On average, significant levels of inbreeding depression were observed for median life span and age-specific mortality. For age-specific mortality, the severity of inbreeding depression increased over the life span. We found that a baseline inbreeding load of 0.307 lethal equivalents per gamete affected age-specific mortality, and that this value increased at a rate of 0.046 per day of the life span. With respect to some survivorship parameters, the differentiation of lineages was nonlinear with respect to the inbreeding coefficient, which suggested that nonadditive genetic variation contributed to variation among lineages. These findings provide insights into the genetic basis of longevity as a quantitative trait and have implications regarding the mutationaccumulation evolutionary explanation of senescence. I NBREEDING depression is the loss of fitness that has often been observed within progeny produced by the mating of closely related individuals (Lynch and Walsh 1998). This phenomenon has been a continuing research interest in evolutionary biology, conservation biology, and the genetic analysis of quantitative traits (Lande and

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

“…Swindell and Bouzat 2006a;Vermeulen et al 2008;Bilde et al 2009). Lifespan is assumed to be extremely sensitive to a large number of environmental factors and it is therefore considered a suitable trait for studies investigating the effects that environmental factors can exert on the level of inbreeding depression (Vermeulen and Bijlsma 2004 and generally low levels of inbreeding depression on resistance to heat, cold and desiccation stresses have also been reported in D. melanogaster (Mikkelsen et al 2010).…”

“…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).…”

“…The inbreeding load (L) affecting the age-specific mortality rate was estimated as the number of lethal equivalents per gamete (Simmons and Crow, 1977;Lynch and Walsh, 1998;Charlesworth and Charlesworth, 1999) following the methods in Swindell and Bouzat (2006). The inbreeding load (L u(t) ) affecting age specific mortality, u(t), was calculated as…”

“…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).…”