A nonrandom subset of olfactory genes is associated with host preference in the fruit flyDrosophila orena

Abstract

Specialization onto different host plants has been hypothesized to be a major driver of diversification in insects, and traits controlling olfaction have been shown to play a fundamental role in host preferences. A diverse set of olfactory genes control olfactory traits in insects, and it remains unclear whether specialization onto different hosts is likely to involve a nonrandom subset of these genes. Here, we test the role of olfactory genes in a novel case of specialization in Drosophila orena. We report the first population‐level sample of D. orena on the West African island of Bioko, since its initial collection in Cameroon in 1975, and use field experiments and behavioral assays to show that D. orena has evolved a strong preference for waterberry (Syzygium staudtii). We then show that a nonrandom subset of genes controlling olfaction‐–those controlling odorant‐binding and chemosensory proteins–‐have an enriched signature of positive selection relative to the rest of the D. orena genome. By comparing signatures of positive selection on olfactory genes between D. orena and its sister species, D. erecta we show that odorant‐binding and chemosensory have evidence of positive selection in both species; however, overlap in the specific genes with evidence of selection in these two classes is not greater than expected by chance. Finally, we use quantitative complementation tests to confirm a role for seven olfactory loci in D. orena’s preference for waterberry fruit. Together, our results suggest that D. orena and D. erecta have specialized onto different host plants through convergent evolution at the level of olfactory gene family, but not at specific olfactory genes.

Parallel evolution of gene expression between trophic specialists despite divergent genotypes and morphologies

“…Many studies that show parallel adaptation at the gene level describe convergence within pigmentation and skeletal development pathways (Miller et al 2007b;Reed et al 2011;Conte et al 2012;Kronforst et al 2012). Perhaps the architecture of metabolic adaptation is more flexible, having more mutational targets or employing more late-acting developmental regulatory networks that are less constrained than early-acting networks (Kalinka et al 2010;Garfield et al 2013;Martin and Orgogozo 2013;Reddiex et al 2013;Ferna et al 2014;Comeault et al 2017). Our findings highlight the importance of understanding convergence across different biological levels of organization.…”

“…; Comeault et al. ). Our findings highlight the importance of understanding convergence across different biological levels of organization.…”

Fine scale mapping of genomic introgressions within theDrosophila yakubaclade

“…Drosophila yakuba is a human-commensal that is widespread throughout sub-Saharan Africa and is also found on islands in the Gulf of Guinea [38-40]. Drosophila teissieri, like D. yakuba, is also distributed across large portions of the continent but is largely restricted to forests with Parinari (Chrysobalanaceae) trees [41-43]. Drosophila santomea is restricted to the island of Sao Tomé in the Gulf of Guinea.…”

Functional insights from the GC-poor genomes of two aphid parasitoids,Aphidius erviandLysiphlebus fabarum

“…Genes underlying chemosensory reception play important roles in parasitoid mate and 581 host localization(Comeault et al 2017;Nouhaud et al 2018). Several classes of 582 chemosensory genes were annotated separately(Table 4): odorant receptors (ORs) are 583 known to detect volatile molecules, odorant-binding proteins (OBPs) and 584 chemosensory proteins (CSPs) are possible carriers of chemical molecules to sensory 585 neurons, and ionotropic receptors (IRs) are involved in both odorant and gustatory 586 molecule reception.…”