Sexy Mouth Odour? Male Oral Gland Pheromone in the Grain Beetle ParasitoidLariophagus distinguendus(Förster) (Hymenoptera: Pteromalidae)

Abstract

Throughout the animal kingdom, sexual pheromones are used for the attraction of mates and as courtship signals but also enable sexual isolation between species. In the parasitic wasp Lariophagus distinguendus, male courtship behaviour consisting of wing fanning, antennal stroking of the female antenna, and head nodding stimulates female receptivity leading to copulation. Recently L. distinguendus was reported to consist of two different lineages, which are sexually isolated because males fail to elicit receptivity in foreign females. It is unclear, however, which part of the courtship behaviour triggers female receptivity and therefore could be a mechanism causing sexual isolation. Here we show that in L. distinguendus a nonvolatile male oral pheromone is essential to release the female receptivity signal. In contrast, male wing fanning and antennal contact play a minor role. Additionally, the composition of the oral pheromone depends on the developmental host and females learn the composition upon emergence from the host substrate. These results will enable more detailed work on oral sexual pheromones to answer the question of how they are involved in the speciation process of L. distinguendus and other parasitoid species, for a better understanding of the huge biodiversity in this group.

The emergence of ecotypes in a parasitoid wasp: a case of incipient sympatric speciation in Hymenoptera?

“…This mate choice decision by the female is most likely based on the male mandibular pheromone which is applied on the female antennae by the males during courtship [ 114 ]. It must have a genetic basis and can not have been induced by the developmental experience of the females as described for the related L. distinguendus [ 58 ], because all wasps were reared under identical conditions and dissected as pupa from the host prior to hatching.…”

“…The emergence of premating and postmating reproductive barriers between inbreeding strains as first barrier in our population is consistent with Askew’s inbreeding hypothesis [ 39 ], stating that inbreeding could lead to reproductive isolation by genetic drift [ 40 , 41 ]. Alternatively, postmating barriers could also be explained by CI due to qualitative or quantitative differences in the presence of CI-inducing bacteria like Wolbachia , and premating barriers could result from differences in developmental experience influencing mate choice decisions of the females [ 58 ]. However, the influence of CI can be excluded by our data on F1-offspring and F1-sex ration, and the role of experience due to our experimental procedure (see above).…”

“…So far, sympatric speciation was convincingly demonstrated only for three braconid species [ 53 – 56 ]. The most detailed studies on the evolution of reproductive barriers exist for the genera Lariophagus (Chalcidoidea: Pteromalidae) , parasitoids of beetle larvae [ 52 , 57 , 58 ], and Nasonia (Chalcidoidea: Pteromalidae), parasitoids of fly pupae in bird nests or on carrion [ 59 – 65 ]. Because the full genome is sequenced for three Nasonia species [ 66 ], this genus serves as a model for other biological traits, e.g.…”

New species based on the biological species concept within the complex of Lariophagus distinguendus (Hymenoptera, Chalcidoidea, Pteromalidae), a parasitoid of household pests

“…This agrees with other data on reproductive barriers in L. distinguendus (König, Zundel, et al, 2019 ), and with the recent study on reproductive barriers within a population of N. vitripennis (Malec et al, 2021 ), where slight sexual isolation was found between closely related populations and even within a population of the same species. As in N. vitripennis , sexual isolation in L. distinguendus is most likely caused by a mate choice decision of the female, which do not accept males with diverging mandibular pheromones that are applied on the female antennae during courtship (König, Seeger, et al, 2015 ; Ruther & Hammerl, 2014 ). The findings that sexual isolation as reproductive barrier seems to precede ecological isolation challenge the view that sexual selection is only a by‐product of natural selection and should be dropped as unique speciation mechanism (Ritchie, 2007 ; Rundle & Rowe, 2018 ; Safran et al, 2013 ; Scordato et al, 2014 ; Weissing et al, 2011 ).…”

“…These two species, which remain undescribed so far, were provisionally named GW species and DB species after their preferred hosts, the granary weevil Sitophilus granarius (Coleoptera: Curculionidae) L. and the drugstore beetle Stegobium paniceum (Coleoptera: Ptinidae) L., respectively. Barriers between the species are formed by differences in host and habitat preferences, different numbers of chromosomes, sexual and postzygotic isolation, as well as endosymbiont‐induced cytoplasmic incompatibility (CI) caused by the bacterium Spiroplasma (Gokhman et al, 2019 ; König, Krimmer, et al, 2015 ; König, Seeger, et al, 2015 ; König, Zundel, et al, 2019 ; König, Paschke, et al, 2019 ; Pollmann et al, 2022 ). The bacterium Wolbachia , which is known to induce CI as reproductive barrier between Nasonia species (Bordenstein et al, 2001 ; Breeuwer & Werren, 1990 ), was also found in the GW species, but did not cause reproductive isolation (König, Zundel, et al, 2019 ).…”