Abstract
Chromosomal polymorphism is widespread in the Drosophila genus, with extensive evidence supporting its adaptive character in diverse species. Moreover, inversions are the major contributors to the genus chromosomal evolution. The molecular characterization of a reduced number of polymorphic inversion breakpoints in Drosophila melanogaster and Drosophila subobscura supports that their inversions would have mostly originated through a mechanism that generates duplications —staggered double-strand breaks— and has thus the potential to contribute to their adaptive character. There is also evidence for inversion breakpoint reuse at different time scales. Here, we have characterized the breakpoints of two inversions of D. subobscura —O4 and O8— involved in complex arrangements that are frequent in the warm parts of the species distribution area. The duplications detected at their breakpoints are consistent with their origin through the staggered-break mechanism, which further supports it as the prevalent mechanism in D. subobscura. The comparative analysis of inversions breakpoint regions across the Drosophila genus has revealed several genes affected by multiple disruptions due not only to inversions but also to single-gene transpositions and duplications.
Highlights
Our work focusing on five inversions of the E chromosome (Muller’s C element) of D. subobscura that are involved in chromosomal arrangements of the E1+2 complex, has already unveiled that one inversion breakpoint with cytological evidence for having been multiply reused has been multiply reused molecularly, and that a second breakpoint considered to be cytologically shared by two inversions is not coincident at the molecular level[12,14]
The identification and molecular characterization of inversions O4 and O8 breakpoint regions of D. subobscura will further contribute to our understanding of how polymorphic inversions originate and it will pave the road to identify the genetic basis of their adaptive character
We have identified the breakpoints of two inversions —inversions O4 and O8 of the O chromosome— by performing the corresponding chromosomal walks that were guided by the results obtained by in situ hybridization of the different rounds of probes in both non-inverted and inverted chromosomes
Summary
O3 arrangement (grey, the previously characterized inversion O3; blue, inversions O4 and O8). Inversions can originate through (i) the cut-and-paste mechanism, (ii) unequal recombination between repetitive elements, and (iii) staggered double-strand breaks and their subsequent repair. Only the latter mechanism generates segmental duplications at the breakpoints of the inverted arrangement[24]. The molecular structure of these inversions breakpoints and of those of one inversion of the O chromosome (Muller’s E element)[11] has revealed that the staggered-breaks mechanism is probably the most frequently used mechanism to generate inversions in this species. The identification and molecular characterization of inversions O4 and O8 breakpoint regions of D. subobscura will further contribute to our understanding of how polymorphic inversions originate and it will pave the road to identify the genetic basis of their adaptive character. The characterization of these regions across the Drosophila genus will shed light on the extent of breakpoint reuse at different time scales
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