Evidence for selection by male mating success in natural populations of Drosophila pseudoobscura.

Abstract

Gene arrangement frequencies were determined at two stages in the life history of Drosophila pseudoobscura taken from nature. Three po ulations in the central highlands of Mexico were each sampled twice during 1976.Gene arrangement frequencies were measured in adult males and in larvae that were the offspring of females collected at the same time. The adult males were in all likelihood a representative sample of those who fathered the larvae produced by the wild females. Differences in gene arrangement frequency between these two life stages should indicate the operation of natural selection. One-third of our comparisons of common gene arrangement frequencies in males and in larvae from the next generation were statistically significant, as were one-third of our comparisons of total frequency arrays in the two life stages. We consider the components of selection that could produce such frequency changes and reason that male mating success must be the major one. Gene arrangement frequencies in the Mexican populations fluctuate within wide bounds. Selection must act to retain the polymorphism in the face of this flux in gene arrangement frequencies, and we suggest that male mating success plays an important role. One of the early triumphs of ecological genetics was the demonstration that selection in nature could be intense-in fact, one or several orders of magnitude more powerful than the founders of population genetics imagined. No experimental system played a more important role in the analysis of selection than the chromosomal polymorphism for gene arrangements in Drosophila pseudoobscura. In this species a series of inversions on the third chromosome binds large blocks of genes together as units, just as though they were alleles of a single "supergene." Natural selection was first implicated when Dobzhansky (2) showed that the frequencies of certain gene arrangements went through seasonal cycles in two of three populations on Mt. San Jacinto in California; subsequent studies showed that these cycles were repeated in years scattered over a span of 2 decades (3, 4). The frequencies of gene arrangements in the third population on Mt. San Jacinto did not cycle, but between 1939 and 1946 they underwent a directional change that Dobzhansky (5) also ascribed to natural selection. Dobzhansky and Levene (6) then showed that karyotypic frequencies in eggs laid by wild females were generally in accord with Hardy-Weinberg expectations, but that frequencies in wild males were not. They concluded that the karyotypes suffered differential mortality during the transition from fertilized egg to adult fly. That selection on the D. pseudoobscura inversions occurred in nature seemed to be settled, and it was generally taken for granted that viability differences accounted for the major part of it.Some 20 years later, a series of papers by Prout (7-10) stimulated evolutionary biologists to pay greater attention to the various components to fitness. These components determine the separate bits of selection that operate at...

Poisson distribution of male mating success in laboratory populations of Drosophila melanogaster

“…Male reproductive fitness in Drosophila has also been seen to have substantial genetic variation compared to several other components of fitness (Prout, 1971 ;Anderson et al, 1979 ;Brittnacher, 1981 ;Kosuda, 1983 ;Miller & Hedrick, 1993 ;Hughes, 1995). In two of these studies, the genotypes screened were either morphological mutants (Prout, 1971) or karyotypes (Anderson et al, 1979), which in both cases were known to be associated with major fitness effects, making a direct comparison with our populations difficult.…”

“…In two of these studies, the genotypes screened were either morphological mutants (Prout, 1971) or karyotypes (Anderson et al, 1979), which in both cases were known to be associated with major fitness effects, making a direct comparison with our populations difficult. In the other four studies, lines rendered homozygous for entire chromosomes were shown to undergo inbreeding depression for various measures of male mating success (Brittnacher, 1981 ;Kosuda, 1983 ;Miller & Hedrick, 1993 ;Hughes, 1995).…”

“…This constraint is especially evident in the case of females, because it is difficult to assess reproductive output of one female in a group. In the case of males, there is substantial empirical evidence that considerable genetic variance for mating success exists, at least under certain types of conditions, in both field and laboratory populations (Prout, 1971 ;Anderson et al, 1979 ;Brittnacher, 1981 ;Partridge et al, 1985 ;Sharp, 1982Sharp, , 1984Hughes 1995 ; but see also Quezada-Diaz et al, 1992). These results, together with the finding that male mating success tends to be positively correlated with various indices of body size in Drosophila (Partridge & Farquhar, 1983 ;Partridge et al, 1987 ;Markow, 1988), suggest that it is likely that the distribution of male mating success in Drosophila will be non-Poisson, with the variance exceeding the mean.…”

Measuring selective effects of modifier gene polymorphisms on the Bare locus of Drosophila subobscura

“…+ heterozygote is detected in cages of low modifier background (averages of fertility estimates were 0.63 and 0.44 in cages L1 and L2, respectively). This is not an unusual result because there are many cases in the literature where fertility selection is an important component of total selection (Polivanov & Anderson, 1969;Sved & Ayala, 1970;Sved, 1971;Bundgaard & Christiansen, 1972;Anderson et al, 1979). On the other hand, our experimental design for fitness estimation splits total fitness into a component of preadult survival or egg-to-adult viability and into an adult fitness component or fertility.…”

Sexual selection on chromosomal polymorphism in Drosophila subobscura

“…The concept of partitioning the action of natural selection into several fitness components has been an important one in stimulating well-designed experiments demonstrating the significance and relative importance of the various components of natural selection. Contrary to the traditional belief about the action of natural selection was the evidence that the adult male component, instead of viabilities of zygotes, played a decisive role in the genetic make-up of different Drosophila populations (Prout, 1971a, b;Bundgaard and Christiansen, 1972;Anderson et a!., 1979;Brittnacher, 1981). In addition, there is also extensive evidence that sexual selection is an important component in the dynamics of polymorphisms (Anderson and Watanabe, 1974;Anderson and McGuire, 1978;Fontdevila and Méndez, 1979;Anderson and Brown, 1984).…”