Genetic variation in recombination in Drosophila. II. Genetic analysis of a high recombination stock

Abstract

The difference in Gl-Sb recombination frequency between two stocks of Drosophila melanogaster, H and C, has been analysed genetically. (The H stock was obtained by artificial selection for increased recombination.) Chromosome substitution experiments show that all three major chromosome contain genes which contribute to the H-C difference, and that there are significant interactions between the genes on different chromosomes. In particular, the H 2nd chromosome increases recombination on a background of homozygous H and X and 3rd chromosomes, but reduces it if either the X or 3rd is made homozygous for C. The H X chromosome exhibits partial or complete dominance over C, depending on the genetic background, while the H 2nd and 3rd chromosomes have dominant effects. Mapping experiments show that at least two recombination genes are located on chromosome 3, one between h and Gl, the other to the right of st, probably between St and sr. Previous data suggest that the X and 2nd chromosome effects are each contributed by single genes or tightly-linked gene complexes. These results are discussed in relation to previous work on the genetics of recombination, and to the patterns of response to selection described in the accompanying paper. INTRODUCTIONIn the accompanying paper (Charlesworth and Charlesworth, 1985), we described the results of artificial selection on recombination in female Drosophila melanogaster. We also presented the results of some genetic studies of the difference between a line (H), which had responded to selection for increased recombination between the 3rd chromosome markers Gl and Sb,and an unselected control stock (C). The genetic background of each of these stocks was derived largely from an outbred population (IV), founded from wild-caught flies.These genetic studies suggested that all three major chromosomes contributed to the difference in recombination frequency. A small reciprocal effect was shown to be controlled by the grandmaternal nuclear genotype.In this paper, we extend these genetic studies by examining the individual contributions of the X, 2nd and 3rd chromosomes to the differences between the H and C stocks, both in homozygous and heterozygous states. Interactions between these chromosomes are also studied. An attempt to localise the 3rd chromosome genes affecting the recombination effect is described. The results are discussed in relation to previous work on the genetics of recombination. MATERIALS AND METHODSAll experimental procedures were as described in the accompanying paper (Charlesworth and Charlesworth, 1985), except that some experiments involved the measurement of recombination frequencies using vial-reared progenies. For such experiments, 2-pair matings were set up in 3" x 1" vials, and the emerging progeny were counted three times over an 8-day period. Chromosome substitutionsThe stocks used in the assays of individual chromosome effects described in the third section were constructed from the isogenic H (high) and C (control) stocks described in the fourth section o...

Increased recombination frequencies resulting from directional selection for geotaxis in Drosophila

“…However, the observed pattern of recombination changes across the genome does not necessarily reflect directly the distribution of geotaxis or rec-loci. Indeed, in experiments with direct selection for recombination, it has been shown that the response to selection for one specific chromosome• region can result in a spectrum of changes in recom- (Chinnici, 1971;Kidwell, 1972;Charlesworth & Charlesworth, 1985). Based on our data and other evidence (Table 1), it can be generalized that directional selection for any trait for many generations can play an important role in rec-system evolution.…”

“…The main arguments against such an interpretation and in favour of the one presented here are: (i) the unidirectional mode of changes in if in both geo + and geo (which are more than simply two independent replications); (ii) reaction of different genome regions in the same direction; (iii) very high rates of if-reaction are not very common in experiments with direct selection for recombination. In fact, the observed differences between opposite selection lines rarely exceed the two or threefold level (Chinnici, 1971;Kidwell, 1972;Dewees, 1975;Charlesworth & Charlesworth, 1985; but see Turner, 1979); and (iv) good reproducibility of the effects between replications (eight replications for each line tested for each of the three chromosomes).…”

“…Experiments on direct selection for altered recombination frequency (if) can be viewed as strong evidence for genetic polymorphism at rec-loci (Allard, 1963;Chinnici, 1971;Landner, 1971;Kidwell, 1972;Shaw, 1972;Dewees, 1975;Turner, 1979;Charlesworth & Charlesworth, 1985). Thus, the key question is whether selection for fitness traits can affect this variation and produce directed changes in if Despite the keen interest in the problem displayed by theoreticians, it has been poorly studied experimentally and what little evidence has accumulated so far, is almost uncited by them.…”

Experimental evolution across different thermal regimes yields genetic divergence in recombination fraction but no divergence in temperature associated plastic recombination

“…Moreover, it is unknown whether changes in recombination among experimental treatments result from direct selection on recombination frequency itself or as an indirect consequence of selection on other traits. Both increases and decreases in recombination rate have been observed in laboratory selection experiments in which recombination rate itself was successfully subjected to artificial selection (Chinnici 1971;Kidwell 1972;Charlesworth and Charlesworth 1985). However, changes in recombination rate have been also shown to evolve as a correlated response to artificial selection on other characters (Flexon and Rodell 1982;Zhuchenko et al 1985;Korol and Iliadi 1994;Rodell et al 2004).…”

Chromosome polymorphisms affecting recombination and exophenotypic traits in Leptysma argentina (Orthoptera): a populational survey

“…These poly. genes can readily respond to intense directional artificial selection (Shaw, 1972(Shaw, , 1974Charlesworth and Charlesworth, 1985). However, if selection acts with low coefficients-as is probably the case for chiasma frequency adjustment-the response would be improved if there were a major gene or a chromosomal rearrangement that produced a marked effect on chiasma frequency and/or distribution.…”