Chemosensory adaptations of the mountain fly Drosophila nigrosparsa (Insecta: Diptera) through genomics’ and structural biology’s lenses

Abstract

Chemoreception is essential for survival. Some chemicals signal the presence of nutrients or toxins, others the proximity of mating partners, competitors, or predators. Chemical signal transduction has therefore been studied in multiple organisms. In Drosophila species, a number of odorant receptor genes and various other types of chemoreceptors were found. Three main gene families encode for membrane receptors and one for globular proteins that shuttle compounds with different degrees of affinity and specificity towards receptors. By sequencing the genome of Drosophila nigrosparsa, a habitat specialist restricted to montane/alpine environment, and combining genomics and structural biology techniques, we characterised odorant, gustatory, ionotropic receptors and odorant binding proteins, annotating 189 loci and modelling the protein structure of two ionotropic receptors and one odorant binding protein. We hypothesise that the D. nigrosparsa genome experienced gene loss and various evolutionary pressures (diversifying positive selection, relaxation, and pseudogenisation), as well as structural modification in the geometry and electrostatic potential of the two ionotropic receptor binding sites. We discuss possible trajectories in chemosensory adaptation processes, possibly enhancing compound affinity and mediating the evolution of more specialized food, and a fine-tuned mechanism of adaptation.

Distinct Subfamilies of Odorant Binding Proteins in Locust (Orthoptera, Acrididae): Molecular Evolution, Structural Variation, and Sensilla-Specific Expression

“…Nevertheless, a molecular and evolutionary stabilized status can be assigned to locust OBP subfamily I-A and II-A that appear to be subject to purifying selection pressure (Figure 3C ), indicative for conserved chemosensory roles. In addition, the chemosensory adaptation to different habitats supposedly implies positive selection constraints (Cicconardi et al, 2017 ), and several of the locust OBPs appear to reflect such a selection regime (Figure 3C ).…”

“…In Drosophila melanogaster , DmelOBP84a, the only orthologous OBP of locust subfamily II-A is actually among the few OBPs that have been reported to be specifically expressed in sensilla coeloconica (Larter et al, 2016 ). Interestingly, the gene encoding OBP84a is retained in most, if not all, Drosophila species genomes (Cicconardi et al, 2017 ). Moreover, the OBP84a ortholog group in Drosophila species withstands apparent purifying selection pressure (Vieira et al, 2007 ) and converges onto a segregated phylogenetic clade (Cicconardi et al, 2017 ), which is very similar to the locust OBP subfamily II-A.…”

Wolbachia affect behavior and possibly reproductive compatibility but not thermoresistance, fecundity, and morphology in a novel transinfected host, Drosophila nigrosparsa

“…Drosophila nigrosparsa naturally uninfected with Wolbachia was collected from Kaserstattalm in Stubai Valley, Tyrol, Austria (47.13°N, 11.30°E) in 2010 (Kinzner et al, 2018), and the isofemale line iso12 was established (Arthofer et al, 2015; Cicconardi et al, 2017). In this study, a subpopulation of iso12 approximately 60 generations after its establishment was used as the uninfected line nu_0 (Figure 1).…”

Differential gene expression inDrosophila melanogasterandD. nigrosparsainfected with the sameWolbachiastrain

“…As uninfected D. nigrosparsa (nu_0), individuals of isofemale line iso12 were used that had been established using a population at Kaserstattalm, Tyrol, Austria (47.13°N, 11.30°E) in 2010 (Arthofer et al ., 2015; Cicconardi et al ., 2017) and had been maintained in the laboratory for about 60 generations before the founding of line nu_0. w Mel-infection of D. nigrosparsa was achieved as described in (Detcharoen et al ., 2020).…”

“…Drosophila (Drosophila) nigrosparsa is an alpine species found at around 2000 m above sea level in Central and Western Europe (Bächli et al ., 2004). Due to the habitat specificity of D. nigrosparsa , molecular and physiological traits and potential effects of warming temperatures on this species have been studied (Arthofer et al ., 2015; Kinzner et al ., 2016, 2018, 2019; Cicconardi et al ., 2017; Tratter Kinzner et al ., 2019). Wild populations of D. melanogaster are commonly infected with Wolbachia (Verspoor and Haddrill, 2011), while no wild population of D. nigrosparsa infected with Wolbachia has been found to date (M. Detcharoen, unpubl.).…”