Male Psyllids Differentially Learn in the Context of Copulation

Abstract

In the Asian citrus psyllid, Diaphorina citri Kuwayama, stimulatory cuticular hydrocarbons act as sex pheromone attractants. Male psyllids locate aggregations of females using those olfactory cues, as well as vibrational communication on the plant surface. Although previous research has indicated that learning plays a role in modulating female reproductive behaviors in psyllids, it is unknown whether males similarly use learning to increase the likelihood of copulatory success. We used an olfactometer-based bio-assay to study the effects of experience on male response to female odor. First, we compared male attraction to female odor in virgin and previously mated males. Second, we tested the effect of several modes of experience with a novel odor, vanillin, to determine whether mating, feeding, or general environmental exposure elicited a learned response. We found that male attraction to female odor significantly increased after mating experience. In addition, we found that males learn about odor specifically in the context of mating, rather than feeding or general exposure. Electrophysiological measurements of antennal response to odorants confirmed that mating status did not affect the sensitivity of the peripheral nervous system to volatile stimuli implicating learning at the level of the central nervous system. These results suggest that male response to female odor is not an entirely innate behavior. Males may require mating experience with female conspecifics to develop attraction to those olfactory cues produced by the female and in association with the female’s habitat. This adaptive plasticity may allow males to detect females in an ever-changing environment and promote diversification and further specialization on different host genotypes.

Sampling Methods for Detection and Monitoring of the Asian Citrus Psyllid (Hemiptera: Psyllidae)

“…Zagvazdina et al (2015) found that mean responses of D. citri males in mate-seeking bioassays decreased when barometric pressure rose or fell more than 1 standard deviation over a 24-h period. Stockton et al (2017) found that the female-odor attractiveness to male D. citri increases after successful mating. In other Hemiptera, Mazzoni et al (2017) found that male H. halys latency to initiate searching activity was lower for males that reached the female song source than those that missed.…”

Female mate preference in an invasive phytopathogen vector: how learning may influence mate choice and fecundity in Diaphorina citri

“…Males may display increased attraction to female odors after mating experience. This appears to be a learned response and depends on a close association between female odor and mating, as males exposed to a novel odor in the context of feeding or ambient exposure failed to demonstrate attraction to the odor (Stockton et al., ). Other research on male D. citri has shown that blue females are more attractive than gray females (Wenninger & Hall, ).…”

“…For this reason, there is significant need to understand the biology and ecology of this pest species. Previous research has demonstrated that learning plays a role in ecology and behavior of D. citri (Patt et al., ; Stockton et al., , ). Male and female D. citri readily associate novel olfactory and visual stimuli with specific host plant genotypes and appear to prefer the host species with which they have had previous feeding experience (Stockton et al., ).…”

“…Male and female D. citri readily associate novel olfactory and visual stimuli with specific host plant genotypes and appear to prefer the host species with which they have had previous feeding experience (Stockton et al., ). In addition, we recently found that male response to female cuticular odors was not entirely innate (Stockton et al., ). Mating experience with receptive females encouraged attraction toward female‐produced odors (Stockton et al., ).…”

Reproductive interference in insects

“…Learned mate preferences have now been displayed in multiple species (e.g. in Drosophila : Dukas, , Dukas et al ., ; in damselflies: Svensson et al ., ; Verzijden & Svensson, ; in psyllids: Stockton et al ., ). While acquiring a mate preference based on experience may allow for greater species discrimination, there are situations where individuals may actually acquire preferences for the ‘wrong’ mate, for instance, if the focal species is locally rare, or simply outnumbered by the ‘interfering’ species.…”