Food searching behaviour of a Lepidoptera pest species is modulated by the foraging gene polymorphism

Abstract

The extent of damage to crop plants from pest insects depends on the foraging behaviour of the insect's feeding stage. Little is known, however, about the genetic and molecular bases of foraging behaviour in phytophagous pest insects. The foraging gene (for), a candidate gene encoding a PKG-I, has an evolutionarily conserved function in feeding strategies. Until now, for had never been studied in Lepidoptera, which includes major pest species. The cereal stem borer Sesamia nonagrioides is therefore a relevant species within this order with which to study conservation of and polymorphism in the for gene, and its role in foraging -a behavioural trait that is directly associated with plant injuries. Full sequencing of for cDNA in S. nonagrioides revealed a high degree of conservation with other insect taxa. Activation of PKG by a cGMP analogue increased larval foraging activity, measured by how frequently larvae moved between food patches in an actimeter. We found one non-synonymous allelic variation in a natural population that defined two allelic variants. These variants presented significantly different levels of foraging activity, and the behaviour was positively correlated to gene expression levels. Our results show that for gene function is conserved in this species of Lepidoptera, and describe an original case of a single nucleotide polymorphism associated with foraging behaviour variation in a pest insect. By illustrating how variation in this single gene can predict phenotype, this work opens new perspectives into the evolutionary context of insect adaptation to plants, as well as pest management.

Role of the foraging gene in worker behavioral transition in the red imported fire ant, Solenopsis invicta (Hymenoptera: Formicidae)

“…18 In nematodes, the ortholog egl-4 plays an important role in determining phenotypes based on olfactory behavior, 19 development 20 and food-related behaviors. 21 In insects, the for gene has been studied widely and shown to be associated with foraging activity, 22 olfaction, 23 learning and memory, 24 and stress tolerance. [25][26][27] Further studies demonstrated that for genes are associated not only with foraging intensity, but also with polyphenism in several insect species, including fruit flies (Diptera), 28 desert locusts (Orthoptera) 26 and pea aphids (Hemiptera), 29 as well as ants (Hymenoptera).…”

Candidate foraging gene orthologs in a lower termite, Reticulitermes flavipes

“…for also influences traits such as sucrose responsiveness (Scheiner, Sokolowski, & Erber, ), memory (Mery, Belay, So, Sokolowski, & Kawecki, ), aggression (S. Wang & Sokolowski, ), starvation resistance (Hughson, Vesterberg, & Sokolowski, ), and thermotolerance (Dawson‐Scully, Armstrong, Kent, Robertson, & Sokolowski, ). for orthologs have been identified in a variety of insects, including locusts (C. Lucas et al, ), kissing bugs (Marliére et al, ), corn borers (Chardonnet et al, ), aphids (Tarès, Arthaud, Amichot, & Robichon, ), honey bees (Ben‐Shahar, Leung, Pak, Sokolowski, & Robinson, ), and ants (Ingram, Oefner, & Gordon, ; Christophe Lucas, Nicolas, & Keller, ). Among the eusocial Hymenoptera, for orthologs act as both positive (Ben‐Shahar et al, ; Bockoven, Coates, & Eubanks, ; Ingram, Kleeman, & Peteru, ) and negative (Kodaira, Ohtsuki, Yokoyama, & Kawata, ; Tobback et al, ) regulators of foraging, on a species‐specific basis.…”

The cGMP‐dependent protein kinase gene can regulate trail‐following behaviour and locomotion in the termite Reticulitermes chinensis Snyder

“…The results of our multiple amino acid sequence alignments indicated that the gene PKG shared the highest sequence identity with Rffor ‐ α , which is one of PKG type I isoforms, was found recently in the termite R. flavipes (Merchant et al, 2020). Type I PKGs had been reported to be associated with foraging in insects (Allen et al, 2017; Chardonnet et al, 2014; Kodaira et al, 2009; Lucas et al, 2010; Tobback et al, 2008), and Rffor‐α was more functionally associated with foraging than Rffor‐β (the another one of PKG type I isoforms) in R. flavipes (Merchant et al, 2020). Hence, we speculated that PKG is probably related to foraging behaviour of the termite R. chinensis .…”

“…This gene encodes a cGMP‐dependent protein kinase (PKG) (Osborne et al, 1997), and additionally regulates food intake (Allen et al, 2017; Kaun, Riedl, et al, 2007b; Scheiner et al, 2004), learning and memory (Kaun, Hendel, et al, 2007a; Kuntz et al, 2012; Mery et al, 2007; Reaume et al, 2011), sleep (Donlea et al, 2012; Harbison et al, 2017; Raizen et al, 2008), and social behaviours (Foucaud et al, 2013; Kohn et al, 2013; Philippe et al, 2016; Wang & Sokolowski, 2017). In addition, for orthologs have been identified in a variety of insects including honey bees (Ben‐Shahar et al, 2003), ants (Ingram et al, 2005; Lucas et al, 2015), locusts (Lucas et al, 2010) and some other insects (Chardonnet et al, 2014; Marliére et al, 2015; Tarès et al, 2013). A recent study showed that two for orthologs, Rffor‐α and Rffor‐β , were cloned from the termite Reticulitermes flavipes and found that Rffor may play a role in locomotor activity rather than being exclusively linked to foraging (Merchant et al, 2020).…”