Environment Exploration and Colonization Behavior of the Pea Aphid Associated with the Expression of the foraging Gene

Abstract

Aphids respond to specific environmental cues by producing alternative morphs, a phenomenon called polyphenism, but also by modulating their individual behavior even within the same morph. This complex plasticity allows a rapid adaptation of individuals to fluctuating environmental conditions, but the underlying genetic and molecular mechanisms remain largely unknown. The foraging gene is known to be associated with behavior in various species and has been shown to mediate the behavioral shift induced by environmental changes in some insects. In this study, we investigated the function of this gene in the clonal forms of the pea aphid Acyrthosiphon pisum by identifying and cloning cDNA variants, as well as analyzing their expression levels in developmental morphs and behavioral variants. Our results indicate that the expression of foraging changes at key steps of the aphid development. This gene is also highly expressed in sedentary wingless adult morphs reared under crowded conditions, probably just before they start walking and foraging. The cGMP-dependent protein kinase (PKG) enzyme activity measured in the behavioral variants correlates with the level of foraging expression. Altogether, our results suggest that foraging could act to promote the shift from a sedentary to an exploratory behavior, being thus involved in the behavioral plasticity of the pea aphid.

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.…”

Colony‐level behavioural variation correlates with differences in expression of theforaginggene in red imported fire ants

“…The foraging gene ( for ) and its homologs have been shown to influence foraging and related behaviours in a wide variety of organisms (e.g., nematodes (Fujiwara, Sengupta, & McIntire, ), fruit flies (de Belle, Hilliker, & Sokolowski, ), grasshoppers (Lucas, Kornfein, et al ), aphids (Tarès, Arthaud, Amichot, & Robichon, ), honeybees (Ben‐Shahar, ) and harvester ants (Ingram et al., )). The for gene encodes a cGMP‐dependent protein kinase (PKG), which can respond to cGMP signalling to phosphorylate target molecules, triggering a suite of downstream effects.…”

Temperature‐ and food‐dependent foraging gene expression in foragers of the red imported fire ant Solenopsis invicta Buren (Hymenoptera: Formicidae)

“…Insects have adapted to almost all types of habitats on the planet as a result of their behavioural plasticity (Tschinkel, ; Despland & Simpson, ; Muller et al ., ), although such shifts in behaviour are known to be strongly associated with foraging ( for ) genes in some insects (Tarès et al ., ; Tobback et al ., ). The naturally occurring behavioural rover/sitter morphs are reported as alleles of the foraging gene ( for R and for S , respectively), encoding cGMP‐dependent protein kinase (de Belle et al ., ; Osborne et al ., ).…”