Odorant and gustatory receptor diversity and evolution in the stinging wasps, ants, and bees (Hymenoptera: Aculeata)

• Applicants: Dr. Ewald Große-Wilde; Professor Dr. Oliver Niehuis
• Subject Area: Evolution, Anthropology ; Sensory and Behavioural Biology ; Ecology and Biodiversity of Animals and Ecosystems, Organismic Interactions
• Term: from 2016 to 2020
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 328103412

• Final Report Year: 2021

Final Report Abstract

Information about the chemical composition of the environment is of critical importance for any organism. Chemical senses enable, for example, localizing and assessing the quality of food sources, oviposition sites, and reproductive partners. Social insects, such as ants, additionally utilize chemical factors (pheromones) to establish their social behaviors. Insects rely primarily on three types of chemosensory receptors to perceive their chemical environment: olfactory (ORs), gustatory (GRs), and ionotropic receptors. Some Hymenoptera feature remarkable OR and GR repertoire expansions, most notably ants and bees. These expansions have been linked with the ants’ and bees’ eusocial life and the associated necessity to discriminate between various different chemical factors (e.g., trail pheromones). However, since chemoreceptors had not been studied in any lineage of Hymenoptera comparatively closely related to eusocial ants and bees, it was unclear whether or not the extraordinary diversity of chemoreceptors in ants and bees is a derived feature of these two groups. The historical focus on sampling chemoreceptors primarily in eusocial species could additionally have resulted in severely underestimating the ancestral chemoreceptor diversity in stinging wasps (Aculeata). To address whether or not non-eusocial aculeate Hymenoptera closely related to eusocial ants and eusocial bees had smaller chemoreceptor repertoire sized than eusocial ants and bees, we annotated genes encoding odorant (ORs), gustatory, and ionotropic receptors and chemosensory soluble proteins and odorant-binding proteins in transcriptomes of chemosensory tissues and in early draft genomes of apoid wasps. 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 (~ 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. Our results support the view that large chemoreceptor repertoire sizes are not as unique to eusocial Hymenoptera as previously assumed, and that herbivorous Hymenoptera tend to possess smaller OR repertoires than carnivorous, parasitoid, or kleptoparasitic species. To obtain more reliable estimates of the chemoreceptor repertoire size of the last common ancestor of Aculeata, we additionally studied chemoreceptors in transcriptomes and draft genomes in Chrysidoidea (cuckoo wasps and relatives) as well as in Stephanus serrator, a parasitoid wasp lineage closely related to Aculeata. Based on the obtained data, we estimate the ancestral repertoire size of Aculeata to have contained at least 263 olfactory and 45 gustatory receptors. The size of the chemoreceptor repertoire in the last common ancestor was thus considerably larger than previously assumed (i.e., 73 and 13).

Publications

• (2017): Chemoreceptor Gene Evolution in Apoidea. 15th ESITO conference, Cagliary (Italy) (September 17–22, 2017)
  Obiero GF, Pauli T, Hansson BS, Niehuis O, Große-Wilde W
  
• (2019) Chemoreceptor diversity and lineage specific gains and losses in the stinging wasps, ants and bees (Hymenoptera: Aculeata). — Münster Evolutionary Meeting, Münster, October 2018
  Pauli T, Obiero G, Große-Wilde E, Niehuis O
  
• (2019): Phylogenetic analysis of cuckoo wasps (Hymenoptera: Chrysididae) reveals a partially artificial classification at the genus level and a species-rich clade of bee parasitoids. – Systematic Entomology 44: 322–335
  Pauli T, Castillo-Cajas RF, Rosa P, Kukowka S, Berg A, van den Berghe E, Fornoff F, Hopfenmüller S, Niehuis M, Peters RS, Staab M, Strumia F, Tischendorf S, Schmitt T, Niehuis O
  
• (2020): Nachweise von Polistes gallicus (Linnaeus 1767) in Rheinland-Pfalz und Baden-Württemberg (Hymenoptera: Vespidae). – Ampulex 11: 9–13
  Schweitzer F, Reder G, Moris VC, Pauli T, Niehuis O
  
• (2021): Analysis of RNA-seq, DNA target enrichment, and Sanger nucleotide sequence data resolves deep splits in the phylogeny of cuckoo wasps (Hymenoptera: Chrysididae). – Insect Systematics and Diversity 5 (1): 1; 1–14
  Pauli T, Meusemann K, Kukowka S, Sann M, Donath A, Mayer C, Oeyen JP, Ballesteros Y, Berg A, van den Berghe E, Escalona HE, Guglielmino A, Niehuis M, Olmi M, Podsiadlowski L, Polidori C, de Rond J, Rosa P, Schmitt T, Strumia F, Wurdack M, Liu S, Zhou X, Misof B, Peters RS, Niehuis O
  
• (2021): Chemoreceptor diversity in apoid wasps and its reduction during the evolution of the pollencollecting lifestyle of bees (Hymenoptera: Apoidea). – Genome Biology and Evolution 13 (3): 1–18
  Obiero GF, Pauli T, Geuverink E, Veenendaal R, Niehuis O, Große-Wilde E