Evidence of Olfactory and Visual Learning in The Asian Citrus Psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae)

Investigation of the mechanisms underlying learning and memory can be achieved through research on neurobiologically simplified invertebrate species. As such, insects have been used for decades as ideal models of olfactory learning. The current study aimed to investigate the mechanisms of chemosensory attraction in an invasive insect, Diaphorina citri, the Asian citrus psyllid (ACP), through manipulation of olfactory stimuli. After classical conditioning to a non-innate cue (vanilla extract), psyllids displayed enhanced feeding behavior. There was, however, an inverse relationship between olfactory “noise” and feeding behavior. Preliminary data suggests ACP may also be visual learners, as evidenced by trials attempting to condition ACP to the color blue. The data indicate that while learning is possible in ACP, it is easily disrupted. As a result, innate response to host plant stimuli in oligophagous, selective feeding insects may represent the most adaptive means of locating resources

Population genomics of Drosophila suzukii reveal longitudinal population structure and signals of migrations in and out of the continental United States

Drosophila suzukii, or spotted-wing drosophila, is now an established pest in many parts of the world, causing significant damage to numerous fruit crop industries. Native to East Asia, D. suzukii infestations started in the United States (U.S.) a decade ago, occupying a wide range of climates. To better understand invasion ecology of this pest, knowledge of past migration events, population structure, and genetic diversity is needed. In this study, we sequenced whole genomes of 237 individual flies collected across the continental U.S., as well as several sites in Europe, Brazil, and Asia, to identify and analyze hundreds of thousands of genetic markers. We observed strong population structure between Western and Eastern U.S. populations, but no evidence of any population structure between different latitudes within the continental U.S., suggesting there is no broad-scale adaptations occurring in response to differences in winter climates. We detect admixture from Hawaii to the Western U.S. and from the Eastern U.S. to Europe, in agreement with previously identified introduction routes inferred from microsatellite analysis. We also detect potential signals of admixture from the Western U.S. back to Asia, which could have important implications for shipping and quarantine policies for exported agriculture. We anticipate this large genomic dataset will spur future research into the genomic adaptations underlying D. suzukii pest activity and development of novel control methods for this agricultural pes

Phenotypic Plasticity Promotes Overwintering Survival in A Globally Invasive Crop Pest, Drosophila suzukii

Spotted wing drosophila, Drosophila suzukii Matsumura, is a major pest of small fruit worldwide in temperate and subtropical growing regions. In Northern climates, D. suzukii likely overwinters locally under leaf litter and snow pack, but our understanding of the factors affecting thermal susceptibility is limited. While previous investigations of thermal susceptibility in this species have employed conventional static acclimation protocols, we aimed to determine whether gradual cooling, or dynamic acclimation, may extend the limits of known thermal tolerance by more closely approximating naturally occurring shifts in temperature. First, we assessed survival among adult and pupal D. suzukii using static acclimation. Then, we re-assessed survival using a novel dynamic acclimation method. We found that while static acclimation was sufficient to induce cold tolerance, dynamic acclimation significantly improved survival at temperatures as low as −7.5 °C. Following static acclimation, the lower lethal limit of adult D. suzukii was −1.1 °C in winter morphotype (WM) adults compared to 1.7 °C in non-acclimated summer morphotype (SM) adults. Dynamic acclimation reduced the lower limit to −5 °C in SM flies. At the end of our study 50% of WM flies survived 72 h at −7.5 °C. Below 0 °C pupal survival declined significantly regardless of acclimation procedure. However, pupal acclimation improved survival outcomes significantly compared to non-acclimated pupae, suggesting that while juvenile diapause is unlikely, cold hardening likely benefits those flies which may develop into the overwintering WM population. These data suggest that the degree of cold hardening is proportional to the thermal environment, a finding previously unrecognized in this species. Given the economic impact of this pest, these data may have important implications for offseason population monitoring and management. We discuss how phenotypic plasticity may drive geographical range expansion, and the impact of climate change on the spread of this species

The Influence of Learning on Host Plant Preference in a Significant Phytopathogen Vector, Diaphorina citri.

Although specialist herbivorous insects are guided by innate responses to host plant cues, host plant preference may be influenced by experience and is not dictated by instinct alone. The effect of learning on host plant preference was examined in the Asian citrus psyllid, Diaphorina citri; vector of the causal agent of citrus greening disease or huanglongbing. We investigated: a) whether development on specific host plant species influenced host plant preference in mature D. citri; and b) the extent of associative learning in D. citri in the form of simple and compound conditioning. Learning was measured by cue selection in a 2-choice behavioral assay and compared to naïve controls. Our results showed that learned responses in D. citri are complex and diverse. The developmental host plant species influenced adult host plant preference, with female psyllids preferring the species on which they were reared. However, such preferences were subject to change with the introduction of an alternative host plant within 24-48 hrs, indicating a large degree of experience-dependent response plasticity. Additionally, learning occurred for multiple sensory modalities where novel olfactory and visual environmental cues were associated with the host plant. However, males and females displayed differing discriminatory abilities. In compound conditioning tasks, males exhibited recognition of a compound stimulus alone while females were capable of learning the individual components. These findings suggest D. citri are dynamic animals that demonstrate host plant preference based on developmental and adult experience and can learn to recognize olfactory and visual host plant stimuli in ways that may be sex specific. These experience-based associations are likely used by adults to locate and select suitable host plants for feeding and reproduction and may suggest the need for more tailored lures and traps, which reflect region-specific cultivars or predominate Rutaceae in the area being monitored

Previously introduced braconid parasitoids target recent olive fruit fly (Bactrocera oleae) invaders in Hawai’i

Abstract The olive fruit fly Bactrocera oleae (Diptera: Tephritidae) was detected on Maui and Hawai’i Islands in 2019, affecting yields and quality of the state’s emerging olive oil industry. Given previous parasitoid releases to control other invasive frugivorous tephritids in Hawai’i, we were interested in determining whether these parasitoids were naturally targeting recent olive fly invaders in field, if local olive cultivar differences affected parasitization rates, and if there was a seasonal pattern of parasitization that could inform future management decisions. To address these questions, we collected data from olive growing in Hawai’i during 2021 and 2022. During the fruiting season we collected monthly samples and reared out B. oleae in the lab. We detected two previously introduced braconid wasps: first Diachasmimorpha tryoni during 2021 and 2022 and later Fopius arisanus during the 2022 collection. Cultivar effects were limited to a single site in our study, where more D. tryoni were reared from ‘Arbequina’ olives. Seasonality of olive fruit fly and parasitoid activity was earlier in lower elevation sites, as expected based on tree phenology and temperature-dependent insect development. This represents the first report of D. tryoni parasitism activity against B. oleae and may reflect elevational effects combined with the ecological complexity in interactions between multiple invasive arthropod pests, their invasive and cultivated plant hosts, and introduced braconid parasitoids

The Influence of Learning on Host Plant Preference in a Significant Phytopathogen Vector, <i>Diaphorina citri</i>

<div><p>Although specialist herbivorous insects are guided by innate responses to host plant cues, host plant preference may be influenced by experience and is not dictated by instinct alone. The effect of learning on host plant preference was examined in the Asian citrus psyllid, <i>Diaphorina citri</i>; vector of the causal agent of citrus greening disease or huanglongbing. We investigated: a) whether development on specific host plant species influenced host plant preference in mature <i>D</i>. <i>citri</i>; and b) the extent of associative learning in <i>D</i>. <i>citri</i> in the form of simple and compound conditioning. Learning was measured by cue selection in a 2-choice behavioral assay and compared to naïve controls. Our results showed that learned responses in <i>D</i>. <i>citri</i> are complex and diverse. The developmental host plant species influenced adult host plant preference, with female psyllids preferring the species on which they were reared. However, such preferences were subject to change with the introduction of an alternative host plant within 24–48 hrs, indicating a large degree of experience-dependent response plasticity. Additionally, learning occurred for multiple sensory modalities where novel olfactory and visual environmental cues were associated with the host plant. However, males and females displayed differing discriminatory abilities. In compound conditioning tasks, males exhibited recognition of a compound stimulus alone while females were capable of learning the individual components. These findings suggest <i>D</i>. <i>citri</i> are dynamic animals that demonstrate host plant preference based on developmental and adult experience and can learn to recognize olfactory and visual host plant stimuli in ways that may be sex specific. These experience-based associations are likely used by adults to locate and select suitable host plants for feeding and reproduction and may suggest the need for more tailored lures and traps, which reflect region-specific cultivars or predominate Rutaceae in the area being monitored.</p></div

Experience dependent host plant preference.

<p>Shifts in preference after short-term adult experience feeding on the alternative host plant species. The labels “Kept on SO” (sour orange) or “Kept on OJ” (orange jasmine) represent the control groups—<i>D</i>. <i>citri</i> maintained on a single host plant species for the duration of the study. The experimental groups are labeled as “Moved to SO” or “Moved to OJ.” Significant differences between groups at each time point are indicated by different letters (χ² test, α≤0.05).</p

Experimental conditioning procedure.

<p>In single stimulus tests, either blue light or vanillin were paired with the host plant. In compound conditioning, all test groups received simultaneous presentation of the visual and olfactory stimuli.</p

<i>D</i>. <i>citri</i> responses after compound conditioning to six test conditions (a-f).

<p>Gray bars represent the olfactory stimulus (vanillin odor), blue bars represent the visual stimulus (blue light), striped blue and gray bars represent the compound stimulus (vanillin odor + blue light), and white bars indicated a blank control. Asterisks (*) within the bars indicate statistically significant differences within a group selecting arm A or arm B (χ² test, *: < 0.05, **: < 0.01, ***: < 0.001), ****: <0.0001. Asterisks (*) outside the bars indicate differences between a set of naïve and experienced insects for a given test condition (χ² test).</p

Developmental host plant preference.

<p>Differences in female <i>D</i>. <i>citri</i> preference based on natal host plant species. Asterisks within bars indicate statistically significant differences within groups, while asterisks associated with a bracket indicate differences between groups (χ² test, *: < 0.05, **: < 0.01).</p