THE EVOLUTIONARY GENETICS OF MALE LIFE-HISTORY CHARACTERS IN DROSOPHILA MELANOGASTER

Alternative models of the maintenance of genetic variability, theories of life-history evolution, and theories of sexual selection and mate choice can be tested by measuring additive and nonadditive genetic variances of com- ponents of fitness. A quantitative genetic breeding design was used to produce estimates of genetic variances for male life-history traits in Drosophila melanogaster. Additive genetic covariances and correlations between traits were also estimated. Flies from a large, outbred, laboratory population were assayed for age-specific competitive mating ability, age-specific survivorship, body mass, and fertility. Variance-component analysis then allowed the decomposition of phenotypic variation into components associated with additive genetic, nonadditive genetic, and environmental vari- ability. A comparison of dominance and additive components of genetic variation provides little support for an important role for balancing selection in maintaining genetic variance in this suite of traits. The results provide support for the mutation-accumulation theory, but not the antagonistic-pleiotropy theory of senescence. No evidence is found for the positive genetic correlations between mating success and offspring quality or quantity that are predicted by "good genes" models of sexual selection. Additive genetic coefficients of variation for life-history characters are larger than those for body weight. Finally, this set of male life-history characters exhibits a very low correspondence between estimates of genetic and phenotypic correlations. Variation in the life-history characters of organisms has always evoked particular interest among evolutionary ge- neticists. Many of these characters are important components of fitness, such that a directional change in a character will lead to an increase in total fitness. Any genetic variant that confers such an advantage should be rapidly swept to fixation by selection. In general, then, one expects components of fitness to exhibit less heritable variation than other traits. Yet, one feature that consistently emerges from life-history studies is measurable intrapopulation variability for traits such as fertility, longevity, and mating success (Houle 1992). How is this variation maintained in the face of strong se- lection? Does selection itself promote genetic variability, due to a general heterozygote advantage, to frequency-dependent selection, or to a selective regime that varies with time or location? Or does the variability that we see represent the balance between mutational input and selective elimination? Attempts to answer these questions have absorbed much of the effort of evolutionary geneticists for nearly a century. Quantitative genetic studies of life-history traits provide one approach for addressing these fundamental evolutionary questions. Estimates of genetic variability for total fitness are needed to evaluate models of the maintenance of genetic variability in equilibrium populations (Turelli 1988; Kondrashov and Turelli 1992). An example of one hypothesis that can be tested by measuring genetic variation for fitness components is the idea that the variation is maintained by overdominance, or heterozygote advantage. This hypothesis can be tested by comparing the magnitudes of additive and nonadditive ge- netic variance for fitness components (Mukai 1985; Char- lesworth 1987). If overdominance or other forms of balancing