Comparing the Expression of Olfaction-Related Genes in Gypsy Moth (Lymantria dispar) Adult Females and Larvae from One Flightless and Two Flight-Capable Populations

Abstract

In insects, flight and sophisticated olfactory systems go hand in hand and are essential to survival and evolutionary success. Females of many Lepidopteran species have secondarily lost their flight ability, which may lead to changes in the olfactory capabilities of both larval and adult stages. The gypsy moth, Lymantria dispar, an important forest pest worldwide, is currently undergoing a diversification process with three recognized subspecies: the Asian gypsy moth (AGM), Lymantria dispar asiatica; the Japanese gypsy moth (JGM), Lymantria dispar japonica; and the European gypsy moth (EGM), Lymantria dispar dispar. Females of EGM populations from North America have lost their flight capacity whereas the JGM and AGM females are flight capable, making this an ideal system to investigate the relationship between flight and olfaction. We used next-generation sequencing to obtain female antennal and larval head capsule transcriptomes in order to (i) investigate the differences in expression of olfaction-related genes among populations; (ii) identify the most similar protein sequences reported for other organisms through a BLAST search, and (iii) establish the phylogenetic relationships of these sequences with respect to other insect species. Using this approach, we identified 115 putative chemosensory genes belonging to five families of olfaction-related genes. A principal component analysis (PCA) revealed that the gene-expression patterns of female antennal transcriptomes from different subspecies were more similar to one another than to the larval head capsules of their respective subspecies supporting strong chemosensory differences between the two developmental stages. An analysis of the shared and exclusively expressed genes for three populations shows no evidence that loss of flight affects the number or type of genes being expressed. These results indicate either (a) that loss of flight does not impact the olfactory gene repertoire or (b) that the secondary loss of flight in American EGM populations may be too recent to have caused major changes in the genes being expressed. However, we found higher expression values for Clavijo McCormick et al.Gypsy Moth Olfactory Gene Expression most olfaction-related genes in EGM females, suggesting that differences in transcription rates could be an adaptation of flightless females to their chemical environment. Differences in olfactory genes and their expression in the larvae appear to be unrelated to the flight ability of adult females and are likely adaptations to different ecological pressures.

Odorant binding proteins promote flight activity in the migratory insect, Helicoverpa armigera

“…The diverse array of nonolfactory roles for OBPs in Diptera include bacterial-induced haematopoiesis in tsetse flies (Benoit et al, 2017), the transportation of sex-pheromones in Helicoverpa sp. (Sun, Huang, Pelosi, & Wang, 2012) and eggshell formation in the mosquito Aedes aegypti (Marinotti et al, 2014).…”

“…The vital role of chemical cues in host location and oviposition (Bruce & Pickett, 2011;Hansson & Stensmyr, 2011;Mescher & De Moraes, 2015) means that the involvement of a sophisticated olfactory system in migration and flight ability is an attractive proposition (Getahun et al, 2016;McCormick et al, 2017). For example, the odorant receptor family (OR), central to the olfactory system of pterygotes, emerged prior to the evolution of winged flight in insects as an adaptation to terrestrial life (Brand et al, 2016).…”

Divergent behavioural responses of gypsy moth (Lymantria dispar) caterpillars from three different subspecies to potential host trees

“…However, we also speculate that the loss of flight ability by EGM females (prior to the introduction of the EGM to America) 11,12 , and subsequent inability of the females to select suitable hosts, may have been an important factor in EGM larvae developing more sophisticated mechanisms of host selection. Interestingly, a recent transcriptomics study exploring the expression of chemosensory-related genes in larval head capsules 31 found significant differences in the gene expression patterns for these three gypsy moth subspecies, suggesting that differences are not only behavioural but at the perception level as well.…”

“…We recently investigated chemosensory differences among larvae of the three subspecies 31 , but no previous work has examined subspecies variation in larval host-finding behaviour. We hypothesize that larvae from the three subspecies may exhibit differences in host preferences and host-selection behaviour as a result of differences in female flight capacity and ecological factors associated with their distribution ranges (e.g., climate, presence of natural enemies, and available hosts), the current study explored responses of early-instar larvae from lab colonies of the three recognised subspecies to host plants of differing quality.…”

Potential Differences and Methods of Determining Gypsy Moth Female Flight Capabilities: Implications for the Establishment and Spread in Novel Habitats

“…Thus, it could be possible to differentiate between populations containing flight-capable and flightless gypsy moth females by examining olfactory genes. McCormick et al [72] studied the differences between olfaction-related genes in gypsy moth females from one flightless and two flight-capable populations. The flightless population, considered to comprise EGMs, came from New Jersey, USA, while the flight-capable populations had origins in Northern Japan and Far Eastern Russia and were considered to comprise JGMs and AGMs, respectively.…”