Quantitative Genetics of Ovariole Number in Drosophila melanogaster. I. Segregating Variation and Fitness

Abstract

The number of ovarioles of the Drosophila melanogaster ovary is a trait thought to be associated with female fecundity, and therefore is expected to be under strong natural selection. This hypothesis may be tested by examining patterns of genetic and environmental variation for ovariole number in natural populations, and by determining the association between ovariole number and fitness in isogenic lines derived from a natural population. We measured ovariole number, and competitive fitness and its components, for 48 homozygous chromosome 3 substitution lines in a standard inbred background; and body size in a sample of 15 chromosome 3 substitution lines. We found significant segregating genetic variation for ovariole number, with a broad-sense heritability (EP) of 0.403 and correspondingly high coefficients of genetic variation (CV a = 20.8) and residual variation (CV R = 25.3). Estimates of quantitativegenetic parameters for body size (EP = 0.191, CV a = 2.15, and CV R = 3.87) are similar to those previously reported for this trait. Although the isogenic chromosome 3 substitution lines varied significantly for components of fitness, there was no significant linear or quadratic association of ovariole number and body size with fitness. There was, however, highly significant sex X genotypeinteractionfor fitness amongthese lines. This specialcase of genotype X environment interaction for fitness may contribute to the maintenance of genetic variation for fitness in natural populations.

Different Mechanisms Underlie Phenotypic Plasticity and Interspecific Variation for a Reproductive Character in Drosophilids (Insecta: Diptera)

“…Intriguingly, EcR heterozygotes and EcR-usp double heterozygotes show a delay in the onset of TF formation (Hodin and Riddiford 1998), a phenotype similar to that observed in this study for D. mauritiana, D. sechellia, and the Honduras strain of D. simulans. Wayne et al (1997) used a quantitative genetic approach to demonstrate substantial genetic variation for ovariole number in D. melanogaster, confirming previous studies (Robertson 1957;Thomas-Orillard 1975;Boulétreau-Merle et al 1982). Interestingly, Wayne and Mackay (1998) found that mutational heritability (V M /V E ) for ovariole number in these lines was low (on the order of 10 Ϫ4 ), suggesting that a relatively small number of loci might contribute to ovariole number differences.…”

“…Wayne et al (1997) used a quantitative genetic approach to demonstrate substantial genetic variation for ovariole number in D. melanogaster, confirming previous studies (Robertson 1957;Thomas-Orillard 1975;Boulétreau-Merle et al 1982). Interestingly, Wayne and Mackay (1998) found that mutational heritability (V M /V E ) for ovariole number in these lines was low (on the order of 10 Ϫ4 ), suggesting that a relatively small number of loci might contribute to ovariole number differences. In interspecific and interpopulational hybridization experiments, loci on chromosomes 2 and 3, but not on the X chromosome, had substantial effects on ovariole number, both within and between species in the melanogaster species group (Coyne et al 1991;Chakir et al 1995).…”

Reproductive Characteristics of the Flower Breeding Drosophila hibisci Bock (Drosophilidae) in Eastern Australia: Genetic and Environmental Determinants of Ovariole Number

“…This result differed from that found by David (1970) and Bouletreau-Merle et al (1982), who observed a positive correlation between ovariole number and the maximum daily rate of oviposition. The difference between these studies could be based on differences in how female fecundity was measured and further experiments are required to explain the discrepancy (Wayne et al 1997).…”

“…The relationship between ovariole number and fitness has not been well established within any Drosophila species. Wayne et al (1997) studied 45 isogenic lines of D. melanogaster derived from nature but found no correlation between ovariole number and fitness. This result differed from that found by David (1970) and Bouletreau-Merle et al (1982), who observed a positive correlation between ovariole number and the maximum daily rate of oviposition.…”

Mutation, Selection, and the Maintenance of Life-History Variation in a Natural Population

“…Some models for mutationally driven extinction focus entirely on such mutations (Lynch and Gabriel 1990;Lande 1994;Lynch et al 1995). Recent studies with Drosophila have shown that the fitness effects of spontaneous mutations are strongly environment dependent and exhibit strong genotype X environment interaction (Kondrashov and Houle 1994;Fry et al 1996;Fernandez and Lopez-FanjuI1997;Wayne and Mackay 1998), although none of these studies has revealed a class of mutations that are clearly deleterious in one environment and beneficial in another.…”