Function and evolution of a gene family encoding odorant binding-like proteins in a social insect, the honey bee (Apis mellifera)

Abstract

The remarkable olfactory power of insect species is thought to be generated by a combinatorial action of two large protein families, G protein-coupled olfactory receptors (ORs) and odorant binding proteins (OBPs). In olfactory sensilla, OBPs deliver hydrophobic airborne molecules to ORs, but their expression in nonolfactory tissues suggests that they also may function as general carriers in other developmental and physiological processes. Here we used bioinformatic and experimental approaches to characterize the OBP-like gene family in a highly social insect, the Western honey bee. Comparison with other insects shows that the honey bee has the smallest set of these genes, consisting of only 21 OBPs. This number stands in stark contrast to the more than 70 OBPs in Anopheles gambiae and 51 in Drosophila melanogaster. In the honey bee as in the two dipterans, these genes are organized in clusters. We show that the evolution of their structure involved frequent intron losses. We describe a monophyletic subfamily of OBPs where the diversification of some amino acids appears to have been accelerated by positive selection. Expression profiling under a wide range of conditions shows that in the honey bee only nine OBPs are antenna-specific. The remaining genes are expressed either ubiquitously or are tightly regulated in specialized tissues or during development. These findings support the view that OBPs are not restricted to olfaction and are likely to be involved in broader physiological functions.

Comparative genomics of chemosensory protein genes reveals rapid evolution and positive selection in ant-specific duplicates

“…Interestingly, the positively selected sites are not inside the protein molecule, but some are located at the cavity opening and some on the surface of the protein structure. This finding is in agreement with the earlier results that the binding pocket of CSPs is more conservative than the positions of the core protein , but in contrast to results from the honeybee OBP genes, where the positively selected sites were located in the putative binding pocket (Forêt and Maleszka, 2006). Nevertheless, positively selected sites in ant CSP genes can have an effect on the interactions the mature protein has with other molecules like pheromones and other chemicals.…”

“…This is the case in Drosophila OBP (Vieira et al, 2007), OR and GR (Gardiner et al, 2008), and in Acyrthosiphon pisum OBP and CSP (Zhou et al, 2010) gene families. The few exceptions of positive selection are offered by the honeybee OBP gene family where positive selection was detected in one subfamily (so-called C-clade) (Forêt and Maleszka, 2006), and the OR and GR genes in a pea aphid, where the most recent duplicate genes were found to evolve under positive selection (Smadja et al, 2009). One reason for contrasting results can be that commonly the selection analyses in chemosensory genes are restricted to orthologous genes, which are not expected to experience positive selection if they have a conserved function.…”

“…The odorant receptor family varies in size from 54 genes in Drosophila virilis to 299 in the flour beetle Tribolium castaneum (Nozawa and Nei, 2007;Engsontia et al, 2008). The OBP and CSP gene families are smaller, OBP family containing 4-81 genes and CSP 3-22 genes in the insect species studied this far (Forêt and Maleszka, 2006;Forêt et al, 2007;Gong et al, 2007;Vieira and Rozas, 2011). OBPs and CSPs belong to different gene families, but possibly have common evolutionary origin of 380-450 million years ago (Mya) .…”

“…Exceptions are the pea aphid OR and GR gene families, where the most recent expansions evolve under positive selection (Smadja et al, 2009) with ecologically based selection for host plant specialization as the possible driving force. Another case is provided by the honeybee where positive selection is driving the diversification of C-subclade of the OBP gene family (Forêt and Maleszka, 2006).…”

Comparative brain transcriptomic analyses of scouting across distinct behavioural and ecological contexts in honeybees

“…Dopamine and glutamate are known to be involved in novelty-seeking behaviour in vertebrates, including humans [34], and a causal relationship was found between increased glutamate signalling and increased scouting probabilities [15]. A weaker but still causal link has also been shown for dopamine and octopamine [15].…”