Increased mutation in crosses between geographically separated strains of Drosophila melanogaster.

Abstract

Mutator activity associated with the common male recombination (MR) chromosomes in Drosophila melanogaster appears to be suppressed in natural populations. Crosses between geographically separated populations, however, lead to the release of mutator activity as measured by a significant increase in visible mutations. Such an increase in mutation in hybrid individuals may be a powerful factor in inducing or releasing variation in nature, and in more extreme instances may contribute to the separation of microdifferentiated populations. Although genetic variation provides the basis for adaptation to changing environments, an incomplete picture of adaptability is given by measuring levels of variation alone. It is incomplete because it assumes that the rate at which new variants are produced in natural populations is low and essentially constant-assumptions that have been brought into question by studies of mutator factors in Drosophila melanogaster (1-4).Although it is clear that various environmental and genetic factors can influence mutation rates (5), genetic factors have been difficult to study because of the technical problems involved in their identification and in the measurement of their activity in natural populations. Recently, however, the study of mutator activity has been given a significant boost. Hiraizumi (6) found that, contrary to common belief, low levels of recombination can occur in the hybrid male progeny of some wild-caught Drosophila melanogaster strains crossed to laboratory marker stocks. Male recombination (MR) was subsequently found to be correlated with mutator activity, chromosome breakage, hybrid sterility, distortion of segregation, and other genetic events (2, 7). Thus, MR can be used as a simple assay for mutator strains, providing a unique opportunity to survey mutator activity in natural populations. One of the most surprising discoveries to come from these surveys is the finding that the factors responsible for MR activity are extremely common in nature, being found world-wide in up to 100% of the wild isofemale strains tested (2).In considering their potential impact upon the genetic structure of natural populations, a second important discovery was that the activity of mutators appears to be genetically suppressed within any particular population (4,8). Upon crossing a wild strain and a laboratory stock, however, suppression breaks down, resulting in the release of mutator activity and an explosive increase in genetic variation. This breakdown in suppression of mutator activity has been called hybrid release (4). MATERIALS AND METHODSThe objective of this study was to measure the spontaneous mutation rate of sex-linked visible mutations in sampled natural populations and in hybrids produced by crossing individuals from these populations. The following wild-caught isofemale lines were used: M-4 (collected by P. A. Parsons, Melbourne,

A model for spontaneous mutation in Drosophila caused by transposing elements

“…If insertional sites are potentially deleterious, selection could favour any of a wide variety of means of regulation, and genetic analysis of the hybrid dysgenesis system in Drosophi!a melanogaster offers a powerful way to study them. For example, both mutation and chromosome breakage studies confirm that mutator activity is decreased or totally suppressed within a strain, but it is released from suppression in certain crosses between strains (Woodruff et al, 1979;Thompson and Woodruff, 1980). In addition, while mutator factors can be mapped, the large difference between mutation rates in reciprocal crosses shows that the system also has an extra-chromosomal component.…”

Highly variable recessive lethal or nearly lethal mutation rates during germ-line development of male Drosophila melanogaster

“…A similar mating scheme as described above was used successfully in earlier assays for the occurrence of mutation clusters in several laboratories (17,18,(25)(26)(27). It was estimated that lethal or nearly lethal mutations identified by the assay span over about 1,200 genes.…”

Variation in spontaneous mutation and repair in natural population lines of Drosophila melanogaster

“…As an indication of the possible impact of hybrid release on the rate of genetic change in nature, Woodruff and Thompson (1982b, and in preparation) have observed that the progeny from 25 of 90 crosses between natural population lines of D. melanogaster have a significantly higher frequency of spontaneous lethal mutations than do the base populations, and similar values have been observed for spontaneous breakage in hybrid progeny. One consequence of the intraspecific release of mutator activity is that high levels of rare genetic variants observed in hybrid zones (Hunt and Selander, 1973;Avise and Smith, 1974;Kilpatrick and Zimmerman, 1976;Gould and Woodruff, 1978;Sage and Selander, 1979;Smith, 1979;Moran et a!., 1980;Greenbaum, 1981;Hafner, 1982;Peters, 1982;Barton et aL, 1983) may be due to increased rates of mutation (Woodruff et aL, 1979;Thompson and Woodruff, 1980), although intragenic recombination could also explain these variants (Golding and Strobeck, 1983). Support for increased rates of mutation as the cause of the increased genetic variation in hybrid zones comes from the observation that high frequencies of novel chromosome re-arrangements are observed in hybrid zones of grasshoppers and the re-arrangements are derived only from hybrid parents (Shaw et aL, 1983).…”

“…For example, hybridisation among migrants in the large-density winery population might be expected to increase mutation rates by the documented intraspecific hybrid release of mutator activity (Thompson and Woodruff, 1980;Woodruff et a!., 1980;Shaw et a!., 1983). As an indication of the possible impact of hybrid release on the rate of genetic change in nature, Woodruff and Thompson (1982b, and in preparation) have observed that the progeny from 25 of 90 crosses between natural population lines of D. melanogaster have a significantly higher frequency of spontaneous lethal mutations than do the base populations, and similar values have been observed for spontaneous breakage in hybrid progeny.…”