The Genetic Architecture of Life Span and Mortality Rates: Gender and Species Differences in Inbreeding Load of Two Seed-Feeding Beetles

Abstract

We examine the inbreeding load for adult life span and mortality rates of two seed beetle species, Callosobruchus maculatus and Stator limbatus. Inbreeding load differs substantially between males and females in both study populations of C. maculatus-life span of inbred females was 9-13% shorter than the life span of outbred females, whereas the life span of inbred males did not differ from the life span of outbred males. The effect of inbreeding on female life span was largely due to an increase in the slope of the mortality curve. In contrast, inbreeding had only a small effect on the life span of S. limbatus-life spans of inbred beetles were $5% shorter than those of outbred beetles, and there was no difference in inbreeding load between the sexes. The inbreeding load for mean life span was $0.4-0.6 lethal equivalents per haploid gamete for female C. maculatus and $0.2-0.3 for both males and females of S. limbatus, all within the range of estimates commonly obtained for Drosophila. However, contrary to the predictions of mutation-accumulation models, inbreeding load for loci affecting mortality rates did not increase with age in either species, despite an effect of inbreeding on the initial rate of increase in mortality. This was because mortality rates decelerated with age and converged to a mortality plateau for both outbred and inbred beetles.T HE evolution of life span, mortality rates, and patterns of senescence is of substantial interest because there is tremendous variation in these traits at all taxonomic levels (Promislow 1991) and because of the medical implications of understanding the genetics underlying mortality rates. Studies on mice, Drosophila, and Caenorhabditis elegans have identified numerous genes that influence life span and/or rates of senescence (Harshman 2002). Recent studies of life span in Drosophila melanogaster indicate that inheritance of life span can be quite complex, with both dominance and epistasis having significant effects on variation in life span (Harshman 2002;Leips and Mackay 2002;Mackay 2002;Spencer et al. 2003;Spencer and Promislow 2005). These studies also show that the genetic architecture (number of genes and degree of allelic and genic interactions) underlying life span differs between the sexes and depends on the environmental conditions in which individuals are reared.One of the major genetic mechanisms proposed to underlie senescence is the accumulation in populations of late-acting deleterious alleles due to the declining force of selection with increasing age (mutation-accumulation theory) (Hughes and Reynolds 2005). Research has now identified many genes and chromosomal regions (QTL) that affect life span in model organisms but we have few data on the frequency of deleterious alleles affecting life span (De Luca et al. 2003;Carbone et al. 2006). We have less data on the sources of variation in deleterious alleles and the age specificity of expression of those alleles and thus their effects on age-specific mortality rates.Inbreeding studies are a com...

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

“…The genetic architecture underlying variation in adult lifespan of C. maculatus differs substantially between the sexes (Fox et al, 2004c(Fox et al, , 2006. Inbreeding studies within populations show that females have a much higher genetic load (inbreeding load) than do males (Fox et al, 2006;Bilde et al, 2009). Crosses between populations indicate that genes affecting lifespan are primarily autosomal and exhibit substantial dominance for long life in females, but not in males (Fox et al, 2004b), consistent with results from within-population inbreeding studies.…”

“…C. maculatus suffers substantial inbreeding depression throughout development (Tran and Credland, 1995;Fox et al, 2007). Inbreeding has been shown to affect female, but not male, lifespan and adult body size (Tran and Credland, 1995;Fox et al, 2006). Inbreeding also negatively affects female fecundity (Tran and Credland, 1995).…”

“…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). Understanding this diversity of experimental results requires analysis of the sources of variation in age-specific expression in the genetic load.…”

“…Crosses between populations indicate that genes affecting lifespan are primarily autosomal and exhibit substantial dominance for long life in females, but not in males (Fox et al, 2004b), consistent with results from within-population inbreeding studies. There is no evidence that expression of the inbreeding load increases with age in C. maculatus; instead, the trend is for expression of the inbreeding load to decrease with age (Fox et al, 2006). However, these earlier studies were all conducted with beetles reared on high quality hosts and at benign temperatures (25-26 1C).…”

“…This beetle is a commonly used model for demographic studies of aging, senescence and the cost of reproduction (M ller et al, 1989a, b, 1990Tatar et al, 1993;Carey, 1994, 1995;Messina and Slade, 1999;Fox and Moya-Larañ o, 2003;Fox et al, 2003aFox et al, , b, 2004aFox et al, , b, 2006. The genetic architecture underlying variation in adult lifespan of C. maculatus differs substantially between the sexes (Fox et al, 2004c(Fox et al, , 2006. Inbreeding studies within populations show that females have a much higher genetic load (inbreeding load) than do males (Fox et al, 2006;Bilde et al, 2009).…”