The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. I. Element frequencies and distribution.

Data were collected on the distribution of nine families of transposable elements among second and third chromosomes isolated from a natural population of Drosophila melanogaster, by means of in situ hybridization of element probes to polytene chromosomes. It was found that the copy numbers per chromosome in the distal sections of the chromosome arms followed a Poisson distribution. Elements appeared to be distributed randomly along the distal sections of the chromosome arms. There was no evidence for linkage disequilibrium in the distal sections of the chromosomes, but some significant disequilibrium was detected in proximal regions. There were many significant correlations between different element families with respect to the identity of the sites that were occupied in the sample. There were also significant correlations between families with respect to sites at which elements achieved relatively high frequencies. Element frequencies per chromosome band were generally low in the distal sections, but were higher proximally. These results are discussed in the light of models of the population dynamics of transposable elements. It is concluded that they provide strong evidence for the operation of a force or forces opposing transpositional increase in copy number. The data suggest that the rate of transposition per element per generation is of the order of 10(-4), for the elements included in this study.

The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. II. Inferences on the nature of selection against elements.

Data were collected on the distribution of nine families of transposable elements among a sample of autosomes isolated from a natural population of Drosophila melanogaster, by means of in situ hybridization of biotinylated probes to polytene chromosomes. There is no general tendency for elements to accumulate at the tips of chromosomes. Elements tend to be present in excess of random expectation in the euchromatin proximal to the centromeres of the major autosomes, and on chromosome four. There is considerable heterogeneity between different families in the extent of this excess. The overall abundance of element families is inversely related to the extent to which they accumulate proximally. The level of proximal accumulation for the major autosomes is similar to that on the fourth chromosome, but less than that for the X chromosome. There is an overall deficiency of elements in the mid-section of the X compared with the mid-sections of the major autosomes, with considerable heterogeneity between families. The magnitude of this deficiency is positively related to the extent to which elements accumulate proximally. No such deficiency is seen if the proximal regions of the X and autosomes are compared. There is a small and non-significant excess of elements in third chromosomes carrying inversions. There is some between-year heterogeneity in element abundance. The implications of these findings are discussed, and it is concluded that they generally support the hypothesis that transposable element abundance is regulated primarily by the deleterious fitness consequences of meiotic ectopic exchange between elements. If this is the case, such exchange must be very infrequent in the proximal euchromatin, and the elements detected in population surveys of this kind must be inserted into sites where they have negligible mutational effects on fitness.

A study of ten families of transposable elements on X chromosomes from a population of Drosophila melanogaster.

Data were collected on the distribution of ten families of transposable elements among fourteen X chromosomes isolated from a natural population of Drosophila melanogaster, by means of in situ hybridization to polytene chromosomes. It was found that, with the exception of roo, the copy number per chromosome followed a Poisson distribution. There was no evidence for linkage disequilibrium, either within or between families. Some pairs of families of elements were correlated with respect to the identity of the sites that were occupied in the sample, although there was no evidence for a correlation with respect to the sites at which elements attained relatively high frequencies. Elements appeared to be distributed randomly along the distal part of the X chromosome. There was, however, a strong tendency for elements to accumulate at the base of the chromosome. Element frequencies per chromosome band were generally low, except at the base of the chromosome where bands in subdivisions 19E and 20A sometimes had high frequencies of occupation. These results are discussed in the light of models of the population dynamics of transposable elements. It is concluded that they provide strong evidence for the operation of a force or forces opposing transpositional increase in copy number. The accumulation of elements at the base of the chromosome is consistent with the idea that unequal exchange between elements at non-homologous sites is such a force, although other possibilities cannot be excluded at present. The data suggest that the rate of transposition per element per generation is of the order of 10(-4), for the elements included in this study.