APPARENT DIRECTIONAL SELECTION OF BODY SIZE IN DROSOPHILA BUZZATII: LARVAL CROWDING AND MALE MATING SUCCESS

The multivariate phenotypic approach of natural selection suggests that selection can be adequately described by combining measurements of selection on phenotypic traits and estimates of heritabilities and genetic correlations (Lande and Arnold 1983). Under this framework (i.e., ignoring the consequences of pleiotropic effects of unconditionally deleterious mutations), two conclusions can be reached when directional selection on a genetically variable trait is detected: (1) that the population is not at an evolutionary equilibrium; or (2) that if the population is indeed at equilibrium, then there exists a "trade-off" between opposing selective forces (see also Robertson 1955). However, when external, nonheritable traits are included in this multivariate approach, a third conclusion is also possible, namely that an apparent selection differential can persist at equilibrium (i.e., without a genetic response) due to a correlation between the nonheritable and the heritable, phenotypic trait (Price et al. 1988; Kirkpatrick et al. 1990; Rausher 1992; van Tienderen and de Jong 1994). Natural selection on body size has long been of interest in Drosophila as well as in other insects. Several laboratory studies have shown a positive phenotypic correlation between adult body size and fitness components in Drosophila (Partridge and Fowler 1993 and references therein), and Wilkinson (1987) provided indirect evidence that the selection favoring large adult flies is countered by the advantage of faster developing larvae that produce genetically smaller adults. Subsequently, Partridge and Fowler (1993), and Santos et al. (1992a, 1994) showed that D. melanogaster flies artificially selected for large body size had a longer development time and a lower viability under high larval densities than their corresponding control lines. The results of these studies show that body size is heritable and suggest that there is a tradeoff between the performance of adult and juvenile stages. A positive phenotypic correlation between male size and mating success has also been found in the field for several Drosophila species (Partridge et al. 1987b; Markow 1988; Santos et al. 1988, 1992b; Taylor and Kekic 1988; James and Jaenike 1992; Markow and Ricker 1992). Wild flies are usually highly variable for body size. Even though there is a genetic component to this variability, much of it is environmental in origin. Thus, Prout and Barker (1989) and Santos et al. (unpubl. manuscript), working with D. buzzatii, showed that approximately 50% of the phenotypic variance in body size is due to differences between rot means (i.e., individual rotting cactus cladodes used as breeding sites), and more than 95% of the between-rot component and 70% of the withinrot component of the phenotypic variance is attributable to environmental causes, most likely differences in larval food supply and fluctuations in temperature across rots. It is thus quite possible that the mating success of a wild male, which is presumably a function of the time it spends in outcompeting other males and in pursuing females (Partridge et al. 1987a), will be influenced by external conditions such as the quantity and energetic quality of food consumed by the individual at the larval stage that, in turns, has effects on its final size. Leibowitz et al. (1995) have recently addressed whether the phenotypic differences between wild caught mating and single D. buzzatii males could be attributable to genetic differences between the samples. Though the laboratory-reared progeny of the mating males were on average larger (but not significantly so), less phenotypically variable, and developed faster than those of single males, their results did not provide clear evidence for directional selection acting on the genetic component of body size, and could be explained by assuming that the mating males carry a lower than average frequency of generally deleterious mutations that affect body size, mating success, and development time. This last interpretation would favor the view that a mutation-selection balance of deleterious alleles with pleiotropic side effects is maintaining additive genetic variation in phenotypic traits (Barton 1990; Kondrashov and Turelli 1992; Gavrilets and de Jong 1993; Caballero and Keightley 1994). It was the aim of the present study to determine the effect of environmentally induced variation of body size on male mating success in D. buzzatii, and to test whether or not this trait responds to phenotypic selection when environmental factors may affect both phenotype and fitness. Briefly, I will show that a male's body size (as measured by wing length) has no impact on mating success in competition among males that grew up under uncrowded conditions, but that size is important among males that grew up under crowded conditions. The phenotypic directional selection on wing length, however, did not translate into a genetic response when the distributions of body size among the offspring were compared.