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

Identifieur interne : 000377 ( Pmc/Curation ); précédent : 000376; suivant : 000378

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

Auteurs : Dara G. Stockton [États-Unis] ; Xavier Martini [États-Unis] ; Joseph M. Patt [États-Unis] ; Lukasz L. Stelinski [États-Unis]

Source :

RBID : PMC:4773162

Abstract

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.


Url:
DOI: 10.1371/journal.pone.0149815
PubMed: 26930355
PubMed Central: 4773162

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<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,
<italic>Diaphorina citri</italic>
; 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
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<italic>citri</italic>
; and b) the extent of associative learning in
<italic>D</italic>
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<italic>citri</italic>
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
<italic>D</italic>
.
<italic>citri</italic>
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
<italic>D</italic>
.
<italic>citri</italic>
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<name>
<surname>Stockton</surname>
<given-names>Dara G.</given-names>
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<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
<xref ref-type="corresp" rid="cor001">*</xref>
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<name>
<surname>Martini</surname>
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<xref ref-type="aff" rid="aff001">
<sup>1</sup>
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<name>
<surname>Patt</surname>
<given-names>Joseph M.</given-names>
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<sup>2</sup>
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<name>
<surname>Stelinski</surname>
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<sup>1</sup>
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<aff id="aff001">
<label>1</label>
<addr-line>Department of Entomology and Nematology, University of Florida, Citrus Research and Education Center, Lake Alfred, Florida, United States of America</addr-line>
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<label>2</label>
<addr-line>United States Department of Agriculture, Agricultural Research Services, U.S. Horticultural Research Laboratory, Ft. Pierce, Florida, United States of America</addr-line>
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<name>
<surname>Renou</surname>
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<xref ref-type="aff" rid="edit1"></xref>
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</contrib-group>
<aff id="edit1">
<addr-line>INRA-UPMC, FRANCE</addr-line>
</aff>
<author-notes>
<fn fn-type="conflict" id="coi001">
<p>
<bold>Competing Interests: </bold>
The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con" id="contrib001">
<p>Conceived and designed the experiments: DGS LLS JMP XM. Performed the experiments: DGS. Analyzed the data: DGS XM. Contributed reagents/materials/analysis tools: LLS. Wrote the paper: DGS XM LLS JMP.</p>
</fn>
<corresp id="cor001">* E-mail:
<email>dara.stockton@ufl.edu</email>
</corresp>
</author-notes>
<pub-date pub-type="epub">
<day>1</day>
<month>3</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection">
<year>2016</year>
</pub-date>
<volume>11</volume>
<issue>3</issue>
<elocation-id>e0149815</elocation-id>
<history>
<date date-type="received">
<day>14</day>
<month>8</month>
<year>2015</year>
</date>
<date date-type="accepted">
<day>4</day>
<month>2</month>
<year>2016</year>
</date>
</history>
<permissions>
<license xlink:href="https://creativecommons.org/publicdomain/zero/1.0/">
<license-p>This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the
<ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/publicdomain/zero/1.0/">Creative Commons CC0</ext-link>
public domain dedication.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:type="simple" xlink:href="pone.0149815.pdf"></self-uri>
<abstract>
<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,
<italic>Diaphorina citri</italic>
; 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
<italic>D</italic>
.
<italic>citri</italic>
; and b) the extent of associative learning in
<italic>D</italic>
.
<italic>citri</italic>
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
<italic>D</italic>
.
<italic>citri</italic>
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
<italic>D</italic>
.
<italic>citri</italic>
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>
</abstract>
<funding-group>
<funding-statement>This research was funded by the University of Florida and the Citrus Research and Development Foundation to LLS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement>
</funding-group>
<counts>
<fig-count count="6"></fig-count>
<table-count count="2"></table-count>
<page-count count="17"></page-count>
</counts>
<custom-meta-group>
<custom-meta id="data-availability">
<meta-name>Data Availability</meta-name>
<meta-value>All relevant data are within the paper and its Supporting Information files.</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
<notes>
<title>Data Availability</title>
<p>All relevant data are within the paper and its Supporting Information files.</p>
</notes>
</front>
</pmc>
</record>

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