The origin of chromosomal inversions as a source of segmental duplications in the Sophophora subgenus of Drosophila

Abstract

Chromosomal inversions can contribute to the adaptation of organisms to their environment by capturing particular advantageous allelic combinations of a set of genes included in the inverted fragment and also by advantageous functional changes due to the inversion process itself that might affect not only the expression of flanking genes but also their dose and structure. Of the two mechanisms originating inversions —ectopic recombination, and staggered double-strand breaks and subsequent repair— only the latter confers the inversion the potential to have dosage effects and/or to generate advantageous chimeric genes. In Drosophila subobscura, there is ample evidence for the adaptive character of its chromosomal polymorphism, with an important contribution of some warm-climate arrangements such as E1+2+9+12. Here, we have characterized the breakpoints of inversion E12 and established that it originated through the staggered-break mechanism like four of the five inversions of D. subobscura previously studied. This mechanism that also predominates in the D. melanogaster lineage might be prevalent in the Sophophora subgenus and contribute to the adaptive character of the polymorphic and fixed inversions of its species. Finally, we have shown that the D. subobscura inversion breakpoint regions have generally been disrupted by additional structural changes occurred at different time scales.

Multiple and diverse structural changes affect the breakpoint regions of polymorphic inversions across the Drosophila genus

“…This is however a laborious endeavor that in the absence of a medium to high quality reference genome sequence of the species under study requires the availability of either other genomic resources such as BAC libraries to narrow down the region under scrutiny, or a good reference genome of a relatively closely related species to use as a guide. The number of polymorphic inversions with breakpoints molecularly characterized is still scanty for Drosophila species4567891011121314. Only in D. melanogaster with one of the best reference genomes, the availability of population genome-wide datasets has allowed to bioinformatically identify the breakpoints of nine polymorphic inversions1516171819.…”

“…Moreover, the molecular structure of these inversions breakpoints and of those of one inversion of the O chromosome (Muller’s E element)11 has also revealed that the staggered-breaks mechanism is probably the most frequently used mechanism to generate inversions in this species. Finally, the comparative analysis of the breakpoint regions of the D. subobscura polymorphic inversions across the Drosophila genus has revealed that some of these regions have been multiply disrupted121314.…”

Drosophila Chromosomal Polymorphism: From Population Aspects to Origin Mechanisms of Inversions

“…In addition, duplicate regions in these events range from a few hundred base pairs to about 8 Kbp (see Table 1), encompassing whole and partial genes in some of these duplications. However, no dose effect or generation of new transcripts was detected in the analyses [61,[84][85][86][87].…”

“…These inversions give rise to the complex arrangements E 1 + 2 , E 1 + 2 + 9 , E 1 + 2 + 9 + 3, and E 1 + 2 + 9 + 12 . These chromosome constitutions, besides providing a great system for the analysis of the mechanisms of origin of inversions, also provide a basis for studying the reuse of the inversion breakpoints at the molecular level [61,[85][86][87].…”

“…yakuba Burla, 1954 [59]; and the chromosomal polymorphism of the E and O chromosomes of D. subobuscura [61,[84][85][86][87]. The study of Ranz et al [59] analyzed the breakpoints of 29 interspecific inversions in these species through experimental and computational methods.…”