Genomics of Natural Populations: How Differentially Expressed Genes Shape the Evolution of Chromosomal Inversions inDrosophila pseudoobscura

Abstract

Chromosomal rearrangements can shape the structure of genetic variation in the genome directly through alteration of genes at breakpoints or indirectly by holding combinations of genetic variants together due to reduced recombination. The third chromosome of Drosophila pseudoobscura is a model system to test hypotheses about how rearrangements are established in populations because its third chromosome is polymorphic for >30 gene arrangements that were generated by a series of overlapping inversion mutations. Circumstantial evidence has suggested that these gene arrangements are selected. Despite the expected homogenizing effects of extensive gene flow, the frequencies of arrangements form gradients or clines in nature, which have been stable since the system was first described >80 years ago. Furthermore, multiple arrangements exist at appreciable frequencies across several ecological niches providing the opportunity for heterokaryotypes to form. In this study, we tested whether genes are differentially expressed among chromosome arrangements in first instar larvae, adult females and males. In addition, we asked whether transcriptional patterns in heterokaryotypes are dominant, semidominant, overdominant, or underdominant. We find evidence for a significant abundance of differentially expressed genes across the inverted regions of the third chromosome, including an enrichment of genes involved in sensory perception for males. We find the majority of loci show additivity in heterokaryotypes. Our results suggest that multiple genes have expression differences among arrangements that were either captured by the original inversion mutation or accumulated after it reached polymorphic frequencies, providing a potential source of genetic variation for selection to act upon. These data suggest that the inversions are favored because of their indirect effect of recombination suppression that has held different combinations of differentially expressed genes together in the various gene arrangement backgrounds.

Gene regulatory divergence between locally adapted ecotypes in their native habitats

“…The enrichment of gene expression differences in our study is consistent with patterns found in inversions between chimpanzees and humans (Marquès‐Bonet et al., ) and Drosophila (Fuller et al., ; Said et al., ), but contrasts with results for the plant Boechera stricta (Lee et al., ). While the finding of an enrichment of differential gene expression for inversions in this study and others is consistent with the supergene hypothesis of inversion evolution, it is by no means definitive proof.…”

“…Global gene expression analyses offer one way to test whether inversions hold together haplotypes of genetic variation potentially responsible for phenotypic divergence between locally adapted populations. Research in a few systems has found evidence of increased levels of expression divergence in inversions (Cassone et al., ; Fuller, Haynes, Richards, & Schaeffer, ; Marquès‐Bonet et al., ). For example, Marquès‐Bonet et al.…”

Widespread gene duplication and adaptive evolution in the RNA interference pathways of the Drosophila obscura group

“…In case segregating weakly-deleterious variants had led to a downward bias in estimates of α, we repeated this analysis excluding all alleles with a minor allele frequency <0.125 [44], although this reduced power to the extent that few genes remained individually significant (Additional file 5 Table S3). We also repeated the analysis with a larger dataset PRJNA326536 [45] (Additional file 5 Table S3), and obtained qualitatively similar results (R 2 =0.946 for α estimates between the analyses; the second dataset, while larger, is less suitable for analysis as only the third chromosome is a direct sample from a wild population).…”

Chromosomal inversions and ecotypic differentiation in Anopheles gambiae: the perspective from whole‐genome sequencing

“…; Fuller et al . ; Mack et al . ), transcriptional profiling could constitute a complementary approach to identifying candidate genes that would not be subject to the same limitation.…”