Reduced natural selection associated with low recombination in Drosophila melanogaster

Synonymous codons are not used equally in many organisms, and the extent of codon bias varies among loci. Earlier studies have suggested that more highly expressed loci in Drosophila melanogaster are more biased, consistent with findings from several prokaryotes and unicellular eukaryotes that codon bias is partly due to natural selection for translational efficiency. We link this model of varying selection intensity to the population-genetics prediction that the effectiveness of natural selection is decreased under reduced recombination. In analyses of 385 D. melanogaster loci, we find that codon bias is reduced in regions of low recombination (i.e., near centromeres and telomeres and on the fourth chromosome). The effect does not appear to be a linear function of recombination rate; rather, it seems limited to regions with the very lowest levels of recombination. The large majority of the genome apparently experiences recombination at a sufficiently high rate for effective natural selection against suboptimal codons. These findings support models of the Hill-Robertson effect and genetic hitchhiking and are largely consistent with multiple reports of low levels of DNA sequence variation in regions of low recombination.      

Hybrid dysgenesis-induced response to selection in Drosophila melanogaster

In Drosophila melanogaster, the P-M and I-R systems of hybrid dysgenesis are associated with high rates of transposition of P and I elements, respectively, in the germlines of dysgenic hybrids formed by crossing females of strains without active elements to males of strains containing them. Transposition rates are not markedly accelerated in the reciprocal, nondysgenic hybrids. Previous attempts to evaluate the extent to which hybrid dysgenesis-mediated P transposition contributes to mutational variance for quantitative characters by comparing the responses to selection of P-M dysgenic and nondysgenic hybrids have given variable results. This experimental design has been extended to include an additional quantitative trait and the I-R hybrid dysgenesis system. The selection responses of lines founded from both dysgenic and nondysgenic crosses showed features that would be expected from the increase in frequency of initially rare genes with major effects on the selected traits. These results differ from those of previous experiments which showed additional selection response only in lines started from dysgenic crosses, and can be explained by the occasional occurrence of large effect transposable element-induced polygenic mutations in both dysgenic and nondysgenic selection lines. High rates of transposition in populations founded from nondysgenic crosses may account for the apparently contradictory results of the earlier selection experiments, and an explanation is proposed for its occurrence.     

Selection and recombination in Drosophila melanogaster

Summary Artificial selection for wing length in Drosophila melanogaster resulted in changed crossing-over frequencies between three marker genes on the 2nd chromosome, b, cn and vg.The results suggest that artificial selection is a causal agent in producing the observed changes; moreover it is suggested that the modifications in cross-over frequency are controlled by extra-nuclear factors.Research supported by C.N.R. Consiglio Nazionale delle Ricerche Roma, Grant n. 115.2298.4791.     

Genetic recombination and adaptation to fluctuating environments: selection for geotaxis in Drosophila melanogaster

Heritable variation in fitness is the fuel of adaptive evolution, and sex can generate new adaptive combinations of alleles. If the generation of beneficial combinations drives the evolution of recombination, then the level of recombination should result in changes in the response to selection. Three types of lines of Drosophila melanogaster varying in their level of genetic recombination were selected over 38 generations for geotaxis. The within-chromosome recombination level of these lines was controlled for 60% of the genome: chromosome X and chromosome II. The full recombination lines had normal, unmanipulated levels of recombination on these two chromosomes. Conversely, nonrecombination lines had recombination effectively eliminated within the X and second chromosomes. Finally, partial recombination lines had the effective rate of within-chromosome recombination lowered to 10% of natural levels for these two chromosomes. The rate of response to selection was measured for continuous negative geotaxis and for a fluctuating environment (alternating selection for negative and positive geotaxis). All selected Drosophila lines responded to selection and approximately 36% of the response to selection was because of the X and second chromosomes. However, recombination did not accelerate adaptation during either directional or fluctuating selection for geotaxis.     

Time of recombination in the Drosophila melanogaster Oocyte

A test has been carried out to determine if the restrictive temperature (31°) acts to reduce recombination in the temperature-sensitive recombination-deficient genotype rec-1 ²⁶/rec-1 ¹⁶ by reducing or eliminating the synaptonemal complex. Measurements of the length of synaptonemal complexes in heat-treated and untreated stage 1 oocytes, following termination of the temperature-sensitive period, reveal less than a 5% difference, with the greater length present in the treated oocytes. Alterations are not observed in synaptonemal complex distribution within the nucleus or in its fine structure. Parallel genetic studies confirm earlier observations that the restrictive temperature, whose action is confined to a 36-h sensitive period virtually coextensive with premeiotic-S, drastically reduces recombination to 10% of normal. The results are most simply interpreted to mean that the restrictive temperatures acts directly on the recombination process.     

Correlation between recombination frequency and fitness in Drosophila melanogaster

The origin and maintenance of genetic recombination are unsettled evolutionary issues. Genetic variation affecting recombination frequency appears to be pervasive in nature, suggesting that natural selection must increase recombination frequency under some circumstances. However, theoretical arguments and experimental evidence indicate that the frequency of recombination should be reduced by natural selection.A hypothesis not previously explored is that recombination modifiers may directly affect the fitness of their carriers; rather than only indirectly (through the production of recombinant progeny) as generally assumed. We have tested this hypothesis by examining three fitness components (viability, male fertility, and female fecundity) in Drosophila melanogaster homozygous for second chromosomes isolated from a natural population. Then, we have measured the frequency of recombination in flies heterozygous for each wild second chromosome and a chromosome carrying five recessive alleles.The results indicate that genes modulating the frequency of recombination have direct effects on fitness as proposed by the hypothesis. However, the correlation between frequency of recombination and fitness is negative. Thus, the riddle of recombination remains unexplained and, in fact, more puzzling that ever.     

The contributions of the second and third chromosomes to selection response in Drosophila melanogaster

Summary A new approach was made to comparing the contributions to response of chromosomes 2 and 3 of Drosophila in lines selected for high and low sternopleural bristle number.Separate response curves for chromosomes 2 and 3 were obtained from changes in the effect of standard second and third chromosomes marked Cy and Mé which were kept segregating with their wild-type homologues during selection.Dominance interaction between marker and wild chromosomes caused some bias in estimating responses in each direction, but the amount by which the responses diverged in the two directions of selection was relatively free from bias. On a log. scale divergences of chromosomes 2 and 3 were in the ratio 11.7 and their heritabilities realised early in selection were 0.14 and 0.26 respectively.There was interaction between the Cy and the Mé chromosomes which was not altered by the selection. Almost all the responses in the lines could be accounted for by addition of the responses in single chromosomes 2 and 3, chromosomes 1 and 4 making a negligible contribution.Sampling, as a cause of variation between selection lines, was reflected in the variation between them in response in chromosomes 2 and 3.     

Sexual selection and immune function in Drosophila melanogaster

The evolution of immune function depends not only on variation in genes contributing directly to the immune response, but also on genetic variation in other traits indirectly affecting immunocompetence. In particular, sexual selection is predicted to trade-off with immunocompetence because the extra investment of resources needed to increase sexual competitiveness reduces investment in immune function. Additional possible immunological consequences of intensifying sexual selection include an exaggeration of immunological sexual dimorphism, and the reduction of condition-dependent immunological costs due to selection of 'good genes' (the immunocompetence handicap hypothesis, ICHH). We tested for these evolutionary possibilities by increasing sexual selection in laboratory populations of Drosophila melanogaster for 58 generations by reestablishing a male-biased sex ratio at the start of each generation. Sexually selected flies were larger, took longer to develop, and the males were more sexually competitive than males from control (equal sex ratio) lines. We found support for the trade-off hypothesis: sexually selected males were found to have reduced immune function compared to control males. However, we found no evidence that sexual selection promoted immunological sexual dimorphism because females showed a similar reduction in immune function. We found no evidence of evolutionary changes in the condition-dependent expression of immunocompetence contrary to the expectations of the ICHH. Lastly, we compared males from the unselected base population that were either successful (IS) or unsuccessful (IU) in a competitive mating experiment. IS males showed reduced immune function relative to IU males, suggesting that patterns of phenotypic correlation largely mirror patterns of genetic correlation revealed by the selection experiment. Our results suggest increased disease susceptibility could be an important cost limiting increases in sexual competitiveness in populations experiencing intense sexual selection. Such costs may be particularly important given the high intersex correlation, because this represents an apparent genetic conflict, preventing males from reaching their sexually selected optimum.