Gene alterations at Drosophila inversion breakpoints provide prima facie evidence for natural selection as an explanation for rapid chromosomal evolution

Abstract

BackgroundChromosomal inversions have been pervasive during the evolution of the genus Drosophila, but there is significant variation between lineages in the rate of rearrangement fixation. D. mojavensis, an ecological specialist adapted to a cactophilic niche under extreme desert conditions, is a chromosomally derived species with ten fixed inversions, five of them not present in any other species.ResultsIn order to explore the causes of the rapid chromosomal evolution in D. mojavensis, we identified and characterized all breakpoints of seven inversions fixed in chromosome 2, the most dynamic one. One of the inversions presents unequivocal evidence for its generation by ectopic recombination between transposon copies and another two harbor inverted duplications of non-repetitive DNA at the two breakpoints and were likely generated by staggered single-strand breaks and repair by non-homologous end joining. Four out of 14 breakpoints lay in the intergenic region between preexisting duplicated genes, suggesting an adaptive advantage of separating previously tightly linked duplicates. Four out of 14 breakpoints are associated with transposed genes, suggesting these breakpoints are fragile regions. Finally two inversions contain novel genes at their breakpoints and another three show alterations of genes at breakpoints with potential adaptive significance.ConclusionsD. mojavensis chromosomal inversions were generated by multiple mechanisms, an observation that does not provide support for increased mutation rate as explanation for rapid chromosomal evolution. On the other hand, we have found a number of gene alterations at the breakpoints with putative adaptive consequences that directly point to natural selection as the cause of D. mojavensis rapid chromosomal evolution.

Constructing Genetic Linkage Maps Using the Whole Genome Sequence of Pacific Bluefin Tuna (<i>Thunnus orientalis</i>) and a Comparison of Chromosome Structure among Teleost Species

“…Genes at recombination breakpoints occasionally experience a fission or fusion event with other genes during chromosomal inversion, fusion, or translocation. Such a phenomenon has been explained as the mechanism of novel gene birth [49]. Thus, different genes are detected in these boundary regions of Pacific bluefin tuna and medaka.…”

“…Several chromosome pairs and homologous sequence regions between tuna and medaka were in reverse orientation between these two species. Chromosome inversion may have occurred from ectopic recombination between homologous sequences or breakage of chromosomes and erroneous repair of free ends by non-homologous endjoining [49]. Genes at recombination breakpoints occasionally experience a fission or fusion event with other genes during chromosomal inversion, fusion, or translocation.…”

A molecular perspective on a complex polymorphic inversion system with cytological evidence of multiply reused breakpoints

“…The recent detection, also through genome sequence comparison, of inverted duplications at the breakpoints of 5 out of the 8 studied inversions segregating in natural populations of D. melanogaster (Corbett-Detig et al, 2012) would support the Ranz et al (2007) proposal for the melanogaster species group. This proportion does not seem, however, to hold for the repleta group of species, neither for fixed inversions-with inverted duplications in 3 out of 10 fixed inversions (Calvete et al, 2012;Guillén and Ruiz, 2012)-nor for polymorphic inversions in D. buzzatii, where the generating mechanism of the three characterized inversions was ectopic recombination between transposable elements (Cáceres et al, 1999;Casals et al, 2003;Delprat et al, 2009).…”

“…This observation of an asymmetric stagger in the two breakpoints of an inversion is not unique to D. subobscura inversions but extensive to most molecularly characterized inversions. Among the detected exceptions in inverted chromosomes with inverted duplicates corresponding to both breakpoints in non-inverted chromosomes are the five D. melanogaster polymorphic inversions-In(1)A, In(1)Be, In(2R)NS, In(3R)K and In(3R)Payne (Matzkin et al, 2005;-, six of the 18 inversions with inverted duplicates fixed between D. melanogaster and D. yakuba (Ranz et al, 2007), and the 2q inversion fixed in D. mojavensis (Guillén and Ruiz, 2012).…”

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

“…Presence of inverted duplications at the breakpoints of the 2h and 2q inversions; origin of the inversions by staggered breaks [83].…”