Molecular Evidence of Chemical Disguise by the Socially Parasitic Spiny Ant Polyrhachis lamellidens (Hymenoptera: Formicidae) When Invading a Host Colony

Abstract

While most ant species establish a colony independently, some socially parasitic ants build the foundation of their colony by invading other ant (host) colonies and utilizing their labor forces. Many socially parasitic ants disguise their cuticular hydrocarbon (CHC) profile, which is also known as signature mixture for nestmate discrimination, when invading the host colony. Since the strategy of chemical disguise is widespread in socially parasitic ants, elucidating the mechanism of chemical disguise will promote knowledge on the evolutionary history of social parasitism. However, detailed knowledge is still lacking, as the relevant information has only originated from circumstantial evidence, which was obtained from ecological observations. In this study, we investigated the mechanism of chemical disguise in a new queen of a temporary socially parasitic spiny ant (Polyrhachis lamellidens) by measuring its CHC profile, performing a tracing assay with labeled substances, and analyzing gene expression levels. First, after rubbing behavior was observed against the host workers, the CHC profile in P. lamellidens shifted to pronounced peaks that closely resembling that of the host workers. We also observed a reduction in aggressive behaviors by the host ant against P. lamellidens after rubbing behavior was performed. In addition, P. lamellidens acquired artificially-applied labeling substances from host workers through their rubbing behaviors, while gene expression profiling showed the expression of CHC synthesis-related genes did not change during this behavior. These results suggest that P. lamellidens directly obtains host CHCs through rubbing behavior, and these host CHCs enables P. lamellidens to remain disguised during colony invasion.

RNA Extraction from Cumulus Cells for Gene Analysis: The Current Strategy and Review of Literature

“…The BioMasher III (Funakoshi ® , Japan) is formed by a filter tube with an abrasive surface inner wall and combined with a pestle with a textured surface. The pestle in the filtered tube layered on to centrifuge the tube is used for manual grinding [22]. Then, the CC-extracted samples were filtered and placed in the recovery tube.…”

Myxomycetes have an allorecognition system that can only discriminate between intraspecies

“…Ants, as eusocial insects, process the ability to recognize their nest mates through cuticular hydrocarbons. This mechanism can also identify different species and non-nest mates of the same species [20, 21, 22]. This recognition behavior in ants contributes to the survival of the colony as a whole by discriminating between the elimination of external enemies and the communication of information with nest mates.…”

Cuticular Hydrocarbon Profiling by Fractionation and GC-MS in Socially Parasitic Ants

“…These behaviors help the newly mated queen to disguise her CHC profile and match that of the host ants. By disguising the CHC profile of the host ants, the newly mated queen is recognized as a nestmate, allowing her to achieve the early stages of social parasitism ( Tsuneoka and Akino, 2012 ; Iwai et al, 2022 ).…”

“…In addition, reproducing the chemical disguise behavior of socially parasitic ants in the laboratory is necessary. In this paper, we describe a method for CHC extraction and measurement, as well as the induction of chemical disguise by a socially parasitic ant under laboratory conditions, which has been established as an actual experimental system, using P. lamellidens and its host Camponotus japonicus as examples, referring to the practical techniques used in our previous study (on Polyrhachis and Camponotus species) ( Iwai et al, 2022 ; Kurihara et al, 2022 ). In addition, we describe the method for the tracing assay using artificial isotopic substances to confirm the transition of the CHC profile from the host species to a socially parasitic ant.…”

“…This protocol was adapted from our established publication ( Iwai et al, 2022 ; Kurihara et al, 2022 ). We thank Toshiharu Akino for advising the extraction method of the CHC and the critical suggestions, and Kazuharu Arakawa, Masaru Tomita, and Masataka Wakayama for their continuous support and help.…”