Chromosomal inversions are the structural mutations that reverse a segment of a chromosome. Inversions can have various genetic effects such as alteration of gene expression, gene duplication, and suppression of recombination(1). Therefore, inversions can have a major impact on evolutionary change in natural populations, from plants to animals including humans(2). While the associations are known, most of the mechanism of the maintenance of inversions is still a matter of theoretical studies(3, 4).
Drosophila melanogaster has been the model species in this field because inversions could be easily detected by microscopy in the giant polytene salivary gland chromosomes(5). Moreover, the recent advances of genomic technologies enable us to distinguish the maintenance mechanism of inversion empirically.
A GWAS approach based on a panel of inversion-specific SNP markers identified SNPs in strong linkage disequilibrium with specific inversions(6). Many of the SNPs were clearly tracing out of the breakpoints, which indicates that the inversions are under local adaptation(4). Moreover, the fact that these inversions were at intermediate frequencies and that they have latitudinal and seasonal clines are consistent with balancing selection. Another study comparing the gene expression between inversion lines and standard lines demonstrated that each inversion has a significant effect on transcript abundance for hundreds of genes including those on unlinked chromosomes, indicating trans-inversion effect(1). Importantly, synthetic inversions generated by flippase recognition target/flippase recombination system showed that simply reversing the corresponding DNA segments did not result in the large-scale gene expression differences(7).
These results demonstrate that several inversion polymorphisms in this species are shaped and maintained by selection. However, the genetic targets of selection associated with inversion are still poorly understood. Further genome-wide analyses and functional genetic testing may provide major progress to this fundamental question.
[References]
1. E. Lavington, A. D. Kern, The Effect of Common Inversion Polymorphisms In(2L)t and In(3R)Mo on Patterns of Transcriptional Variation in Drosophila melanogaster. G3-Genes Genomes Genetics 7, 3659-3668 (2017).
2. M. Wellenreuther, L. Bernatchez, Eco-Evolutionary Genomics of Chromosomal Inversions. Trends in Ecology & Evolution 33, 427-440 (2018).
3. B. Charlesworth, N. H. Barton, The Spread of an Inversion with Migration and Selection. Genetics 208, 377-382 (2018).
4. R. F. Guerrero, F. Rousset, M. Kirkpatrick, Coalescent patterns for chromosomal inversions in divergent populations. Philosophical Transactions of the Royal Society B-Biological Sciences 367, 430-438 (2012).
5. T. Dobzhansky, A. H. Sturtevant, Inversions in the chromosomes of drosophila pseudoobscura. Genetics 23, 28-64 (1938).
6. M. Kapun, D. K. Fabian, J. Goudet, T. Flatt, Genomic Evidence for Adaptive Inversion Clines in Drosophila melanogaster. Molecular Biology and Evolution 33, 1317-1336 (2016).
7. I. Said et al., Linked genetic variation and not genome structure causes widespread differential expression associated with chromosomal inversions. Proceedings of the National Academy of Sciences of the United States of America 115, 5492-5497 (2018).