Are bigger flies always better : the role of genes and environment ( A commentary on

Body size, especially in invertebrates, is often positively correlated with major fitness components such as female fecundity and male mating success, and it is believed that the evolution of larval growth rate and adult body size in insects is largely shaped by a tradeoff between the fitness benefits of being large versus those of developing to adulthood fast (Santos et al. 1988; Partridge and Fowler 1993). Understanding the phenotypic inter-relationships between development time, body size and adult fitness components in insects, and how these relationships are affected by genotype and environment, is therefore directly relevant to two contentious and central issues in evolutionary genetics: (1) the nature of genetic constraints on the attainment of an optimal life-history, and (2) the relative role of genotypic and environmental variation and covariation in determining the magnitude and sign of phenotypic correlations between fitness related traits (Prasad and Joshi 2003). Almost half a century ago, in a characteristically rigorous and detailed study, Robertson (1957) examined the nature of genetic variation and covariation between body size (thorax length) and egg production (total fecundity between days 4–8 post-eclosion), under benign and uniform rearing conditions, in a large, genetically variable laboratory population of Drosophila melanogaster. The major findings of Robertson’s (1957) study were that (a) there was a significant positive phenotypic correlation between body size and egg production, (b) about 50% of the phenotypic variance in body size was due to genetic variation, mostly additive, (c) about 60% of the phenotypic variance in egg production was due to genetic variation, with a large non-additive component, (d) body size and egg production appeared to be independently genetically correlated with development time, the latter negatively and the former positively, and (e) the genetic correlation underlying the positive phenotypic correlation between body size and egg production was largely non-additive. Quite apart from the significance of the results, there are several appreciable methodological features of Robertson’s (1957) study, features that are important to experimental design and execution in evolutionary genetics but, unfortunately, often overlooked, although practitioners of experimental evolution have recently been repeatedly calling attention to them (e.g. Rose et al. 1996; Ackermann et al. 2001; Chippindale et al. 2003). For example, Robertson (1957) worked with a large, genetically variable, and reasonably well laboratory-adapted population that was close to genetic equilibrium for the traits being studied, explicitly controlled larval density during assays, recognized that trait relationships could be environmentand age-specific and tried to incorporate this knowledge in the choice of measures for size and egg production, and was sensitive to the fact that phenotypic measures of fitness related traits often vary from day to day, and assay to assay, and, consequently, tried to account for that variation in the experimental design and analysis. Except for the lack of population level replication, these precautions, and the caveats one finds throughout Robertson’s (1957) discussion of the results, make for a very ‘modern’ paper in experimental evolutionary genetics, in stark and somewhat unfortunate contrast to many contemporary papers that often seem to be imbued with a combination of an abiding faith in selection as an inexorable optimizing force and an overly simplistic view of the evolutionary process.