Transcriptional responses are oriented towards different components of the rearing environment in two Drosophila sibling species

Abstract

Background The chance to compare patterns of differential gene expression in related ecologically distinct species can be particularly fruitful to investigate the genetics of adaptation and phenotypic plasticity. In this regard, a powerful technique such as RNA-Seq applied to ecologically amenable taxa allows to address issues that are not possible in classic model species. Here, we study gene expression profiles and larval performance of the cactophilic siblings Drosophila buzzatii and D. koepferae reared in media that approximate natural conditions and evaluate both chemical and nutritional components of the diet. These closely related species are complementary in terms of host-plant use since the primary host of one is the secondary of the other. D. koepferae is mainly a columnar cactus dweller while D. buzzatii prefers Opuntia hosts. Results Our comparative study shows that D. buzzatii and D. koepferae have different transcriptional strategies to face the challenges posed by their natural resources. The former has greater transcriptional plasticity, and its response is mainly modulated by alkaloids of its secondary host, while the latter has a more canalized genetic response, and its transcriptional plasticity is associated with the cactus species. Conclusions Our study unveils a complex pleiotropic genetic landscape in both species, with functional links that relate detox responses and redox mechanisms with developmental and neurobiological processes. These results contribute to deepen our understanding of the role of host plant shifts and natural stress driving ecological specialization.

Transposable elements as evolutionary driving force to host shift in cactophilicDrosophilaspecies

“…Although we have species with preferential use for Opuntia and for columnar cacti in both subgroups, D. koepferae and D. buzzatii are adapted to different hosts for a longer time than those of the mulleri complex studied here. In addition, a preliminary study demonstrated that D. buzzatii have a high divergence on larvae gene expression compared to D. koepferae (40), reinforcing the variance that we have observed. In mulleri complex, although not high, it is noteworthy that the subclusters of gene expression from D. m. mojavensis, D. m. baja, D. m. sonorensis, and the subcluster from D. arizonae and D. m. wrigleyi.…”

“…The resolution of gene annotation for D. arizonae was similar to D. mojavensis subspecies due to the recent (1.5 Mya) divergence between them (43), whereas for D. buzzatii and D. koepferae it was ~23% smaller compared to D. mojavensis, as expected since they are more distant related species (44). Similar amount of genes had been annotated previously in the D. buzzatii (45,46) and D. koepferae (46,40) genomes. Since analysis on HLAU genes is the focus of this study, their efficient annotation is relevant.…”

“…Many genes were reported with detoxification, energy production, among others. Another similar study with larvae transcriptome, but with D. buzzatii and D. koepferae , proposed that D. buzzatii flies reared in columnar cacti media have a stronger detoxification response in comparison with D. koepferae flies, suggesting that D. koepferae has a canalized transcriptome response to the toxic alkaloids from columnar cacti (40). We expected to find a higher number of detoxification genes in the subspecies with preference for columnar cacti compared to D. m. wrigleyi and D. buzzatii that use primarily Opuntia sp .…”

“…Many aspects of the HS adaptation in repleta species have been described, such as detoxification pathways (35), morphology (36), life history traits (37), behavior (38), and genomics and transcriptomics (27,(39)(40)(41)(42). However, the contribution of TEs to HLAU genes…”