Chemoreceptor Diversity in Apoid Wasps and Its Reduction during the Evolution of the Pollen-Collecting Lifestyle of Bees (Hymenoptera: Apoidea)

Abstract

Chemoreceptors help insects to interact with their environment, to detect and assess food sources and oviposition sites, and to aid in intra- and inter-specific communication. In Hymenoptera, species of eusocial lineages possess large chemoreceptor gene repertoires compared to solitary species, possibly because of their additional need to recognize nest-mates and caste. However, a critical piece of information missing so far has been the size of chemoreceptor gene repertoires of solitary apoid wasps. Apoid wasps are a paraphyletic group of almost exclusively solitary Hymenoptera phylogenetically positioned between ant and bee, both of which include eusocial species. We report the chemosensory-related gene (CRG) repertoire sizes of three apoid wasps: Ampulex compressa, Cerceris arenaria, and Psenulus fuscipennis. We annotated genes encoding odorant (ORs), gustatory (GRs), and ionotropic (IRs) receptors and chemosensory soluble proteins (CSPs) and odorant-binding proteins (OBPs) in transcriptomes of chemosensory tissues of the above three species and in early draft genomes of two species, A. compressa and C. arenaria. Our analyses revealed that apoid wasps possess larger OR repertoires than any bee lineage, that the last common ancestor of Apoidea possessed a considerably larger OR repertoire (ca. 160) than previously estimated (73), and that the expansion of OR genes in eusocial bees was less extensive than previously assumed. Intriguingly, the evolution of pollen-collecting behavior in the stem lineage of bees was associated with a notable loss of OR gene diversity. Thus, our results support the view that herbivorous Hymenoptera tend to possess smaller OR repertoires than carnivorous, parasitoid, or kleptoparasitic species.

Transcriptome Analysis and Characterization of Chemosensory Genes in the Forest Pest, Dioryctria abietella (Lepidoptera: Pyralidae)

“…With the discovery of three chemosensory receptor gene families in D. melanogaster (Clyne et al, 1999(Clyne et al, , 2000Benton et al, 2009), to date a large number of ORs, GRs and IRs have been identified and characterized in Diptera (Nozawa and Nei, 2007;Croset et al, 2010), Lepidoptera (Engsontia et al, 2014;Xu, 2020;Yin et al, 2021), Coleoptera (Andersson et al, 2019;Mitchell et al, 2020;Mitchell and Andersson, 2021), Hemiptera (Smadja et al, 2009;, and Hymenoptera (Ferguson et al, 2021;Obiero et al, 2021). In insects, ORs are expressed in sensilla basiconica and sensilla trichoidea separately responsible for general odorants (i.e., general ORs) and sex pheromones (i.e., pheromone receptors, PRs) (Krieger et al, 2009;de Fouchier et al, 2017;Guo et al, 2020), while olfactory sensory neurons expressing IRs are distributed in sensilla coeloconica sensitive to amines, acids, alcohols and aldehydes (Yao et al, 2005;Silbering et al, 2011;Rytz et al, 2013).…”

Conserved orthology in termite chemosensory gene families

“…However, high number of ORs has been reported also in non-eusocial Hymenoptera, such as Nasonia vitripennis (301, Robertson et al, 2010), suggesting that the expansion of ORs is an ancestral trait shared by Hymenoptera, which might potentially had facilitated the multiple independent evolutions of eusociality in hymenopteran insects. By contrast, the high OR repertoire reported recently in basal solitary apoid wasps phylogenetically positioned between ants and bees indicates that the OR repertoire in fact reduced during the evolution of eusocial apoids (Obiero et al, 2021). Termites, despite being eusocial insects, exhibit numbers of OR genes comparable to non-eusocial insects (Mitaka and Akino, 2021).…”

“…Chemosensory genes have been identified in a wide range of insects using genomic and transcriptomic approaches (Clyne et al, 1999;Gao and Chess, 1999;Vosshall et al, 1999) which to a large extent enabled us to understand their evolutionary and behavioral adaptations in different contexts of biology including eusociality (Robertson and Wanner, 2006;Zhou et al, 2012Zhou et al, , 2015Engsontia et al, 2014;Terrapon et al, 2014;De Fouchier et al, 2017;Pask et al, 2017;Auer et al, 2020;Obiero et al, 2021;Keesey et al, 2022). Termites, despite being eusocial insects with wellstudied chemical ecology and pheromone biology, have not been examined in detail in this regard until recently, with chemosensory genes identified only in three species: Zootermopsis nevadensis (Archotermopsidae) with 85 ORs in the genome (Terrapon et al, 2014), Cryptotermes secundus (Kalotermitidae) with 42 ORs in the genome (Harrison et al, 2018) and Reticulitermes speratus (Rhinotermitidae) with 22 ORs in the whole-body transcriptome (Mitaka et al, 2016).…”

“…BLASTx searches (Camacho et al, 2009) were performed on these local databases using reference datasets of each multigene family: ORs, IRs, OBPs, CSPs and SNMPs as queries with an e-value cut-off of 0.001. For ORs, reference datasets included amino acid sequences of Z. nevadensis (nr), C. secundus (nr), and D. melanogaster (Refseq NCBI) as well as sequences of Ampulex compressa, Cerceris arenaria, Psenulus fuscipennis, Apis mellifera, Bombus terrestris, Habropoda laboriosa, Dufourea noveangliae, Lasioglossum albipes, Nasonia vitripennis, Harpegnathus saltator, and Solenopsis invicta previously reported in Obiero et al (2021). OR candidate protein sequences were further subject to analysis for presence of the correct transmembrane domains using TMHMM 2.0 (Krogh et al, 2001).…”

Decoding the genetic and chemical basis of sexual attractiveness in parasitic wasps

“…In fact, a couple of studies have already hinted at MB-alkanes as the main carriers for chemical information in insect CHC profiles, providing evidence for the involvement of MB-alkanes in chemical communication processes (35, 36). This might be of particular importance in Hymenoptera, an insect order with CHC profiles largely dominated by MB-alkanes (37, 38) and in which both theoretical considerations as well as empirical evidence have accumulated for the increased complexity and high sophistication of their chemical communication systems (39, 40). Contrary to this, it has been argued that olefins (mainly n -alkenes and dienes) have a higher potential for encoding chemical information than MB-alkanes (41).…”