Journal article 1603 views
Can Insects Develop Resistance to Insect Pathogenic Fungi?
François Leulier,
Ivan M. Dubovskiy,
Miranda M. A. Whitten,
Olga N. Yaroslavtseva,
Carolyn Greig,
Vadim Y. Kryukov,
Ekaterina V. Grizanova,
Krishnendu Mukherjee,
Andreas Vilcinskas,
Viktor V. Glupov,
Tariq Butt 
PLoS ONE, Volume: 8, Issue: 4, Start page: e60248
Swansea University Author:
Tariq Butt
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DOI (Published version): 10.1371/journal.pone.0060248
Abstract
This paper presents new, important information on the microevolution of insect resistance to the insect pathogenic fungus Beauveria bassiana which will have far-reaching implications for the development of insect pathogenic fungi as biological control agents. We placed successive generations of a me...
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2013
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<?xml version="1.0"?><rfc1807><datestamp>2015-06-17T21:28:01.2176632</datestamp><bib-version>v2</bib-version><id>14510</id><entry>2013-04-02</entry><title>Can Insects Develop Resistance to Insect Pathogenic Fungi?</title><swanseaauthors><author><sid>85d1c2ddde272a1176e74978e25ebece</sid><ORCID>0000-0002-8789-9543</ORCID><firstname>Tariq</firstname><surname>Butt</surname><name>Tariq Butt</name><active>true</active><ethesisStudent>false</ethesisStudent></author></swanseaauthors><date>2013-04-02</date><deptcode>SBI</deptcode><abstract>This paper presents new, important information on the microevolution of insect resistance to the insect pathogenic fungus Beauveria bassiana which will have far-reaching implications for the development of insect pathogenic fungi as biological control agents. We placed successive generations of a melanic population of the Greater wax moth, Galleria mellonella, under constant selective pressure from the insect pathogenic fungus, Beauveria bassiana. Enhanced fungal resistance was observed and larvae from the 25th generation were studied in detail to uncover mechanisms underpinning resistance, and the possible cost of those survival strategies. There are 3 novel, core findings from the study:1.Antifungal resistance in these insects is pathogen species-specific, and probably arises through trans-generational immune priming. The resistance was less obvious in earlier generations, suggesting subtle cumulative changes that are only fully apparent in the 25th generation. 2.The insect’s fecundity is already pushed close to minimum by its melanic phenotype. Therefore, the additional drain on resources required to boost antifungal defence still more, comes not from further compromising life history traits but via a re-allocation of the insect’s immune defences. Specifically during B. bassiana infection, systemic (fat body and hemocoel) responses, particularly the expression of antimicrobial peptides, are damped down in favour of a tailored repertoire of enhanced responses in the integument (cuticle and epidermis) – the foremost and most important barrier to natural fungal infection. 3.A previously-overlooked range of putative stress-management factors are activated during the specific response of selected insects to B. bassiana. This too occurs primarily in the integument, and contributes to antifungal defense and/or helps ameliorate the damage inflicted by the fungus or the host’s own immune responses during the battle between host and pathogen.No other study to date has examined so many genes in this context. Indeed, we show that the epidermis has a great capacity to express defense and stress-management genes as well as the fat body (which is the main tissue producing antimicrobial peptides and has been the traditional focus of attention). We therefore propose a “be specific / fight locally / de-stress” model to explain resource allocation and defence priorities for insects selected for superior resistance to insect-pathogenic fungi. However, we also show that these insects are less fecund and probably at no evolutionary advantage in the wild, implying that the risk is small of biological control agents failing in the field.</abstract><type>Journal Article</type><journal>PLoS ONE</journal><volume>8</volume><journalNumber>4</journalNumber><paginationStart>e60248</paginationStart><publisher/><issnPrint/><issnElectronic/><keywords>Insect-pathogenic fungus, Beauveria bassiana, Metarhizium anisopliae, Waxmoth, Galleria mellonella, resistance, immunity, stress response, immune priming, antimicrobial peptides, integument, fat body, biological control agent, microevolution</keywords><publishedDay>31</publishedDay><publishedMonth>12</publishedMonth><publishedYear>2013</publishedYear><publishedDate>2013-12-31</publishedDate><doi>10.1371/journal.pone.0060248</doi><url/><notes/><college>COLLEGE NANME</college><department>Biosciences</department><CollegeCode>COLLEGE CODE</CollegeCode><DepartmentCode>SBI</DepartmentCode><institution>Swansea University</institution><apcterm/><lastEdited>2015-06-17T21:28:01.2176632</lastEdited><Created>2013-04-02T09:45:50.2947202</Created><path><level id="1">Faculty of Science and Engineering</level><level id="2">School of Biosciences, Geography and Physics - Biosciences</level></path><authors><author><firstname>François</firstname><surname>Leulier</surname><order>1</order></author><author><firstname>Ivan M.</firstname><surname>Dubovskiy</surname><order>2</order></author><author><firstname>Miranda M. A.</firstname><surname>Whitten</surname><order>3</order></author><author><firstname>Olga N.</firstname><surname>Yaroslavtseva</surname><order>4</order></author><author><firstname>Carolyn</firstname><surname>Greig</surname><order>5</order></author><author><firstname>Vadim Y.</firstname><surname>Kryukov</surname><order>6</order></author><author><firstname>Ekaterina V.</firstname><surname>Grizanova</surname><order>7</order></author><author><firstname>Krishnendu</firstname><surname>Mukherjee</surname><order>8</order></author><author><firstname>Andreas</firstname><surname>Vilcinskas</surname><order>9</order></author><author><firstname>Viktor V.</firstname><surname>Glupov</surname><order>10</order></author><author><firstname>Tariq</firstname><surname>Butt</surname><orcid>0000-0002-8789-9543</orcid><order>11</order></author></authors><documents/><OutputDurs/></rfc1807> |
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2015-06-17T21:28:01.2176632 v2 14510 2013-04-02 Can Insects Develop Resistance to Insect Pathogenic Fungi? 85d1c2ddde272a1176e74978e25ebece 0000-0002-8789-9543 Tariq Butt Tariq Butt true false 2013-04-02 SBI This paper presents new, important information on the microevolution of insect resistance to the insect pathogenic fungus Beauveria bassiana which will have far-reaching implications for the development of insect pathogenic fungi as biological control agents. We placed successive generations of a melanic population of the Greater wax moth, Galleria mellonella, under constant selective pressure from the insect pathogenic fungus, Beauveria bassiana. Enhanced fungal resistance was observed and larvae from the 25th generation were studied in detail to uncover mechanisms underpinning resistance, and the possible cost of those survival strategies. There are 3 novel, core findings from the study:1.Antifungal resistance in these insects is pathogen species-specific, and probably arises through trans-generational immune priming. The resistance was less obvious in earlier generations, suggesting subtle cumulative changes that are only fully apparent in the 25th generation. 2.The insect’s fecundity is already pushed close to minimum by its melanic phenotype. Therefore, the additional drain on resources required to boost antifungal defence still more, comes not from further compromising life history traits but via a re-allocation of the insect’s immune defences. Specifically during B. bassiana infection, systemic (fat body and hemocoel) responses, particularly the expression of antimicrobial peptides, are damped down in favour of a tailored repertoire of enhanced responses in the integument (cuticle and epidermis) – the foremost and most important barrier to natural fungal infection. 3.A previously-overlooked range of putative stress-management factors are activated during the specific response of selected insects to B. bassiana. This too occurs primarily in the integument, and contributes to antifungal defense and/or helps ameliorate the damage inflicted by the fungus or the host’s own immune responses during the battle between host and pathogen.No other study to date has examined so many genes in this context. Indeed, we show that the epidermis has a great capacity to express defense and stress-management genes as well as the fat body (which is the main tissue producing antimicrobial peptides and has been the traditional focus of attention). We therefore propose a “be specific / fight locally / de-stress” model to explain resource allocation and defence priorities for insects selected for superior resistance to insect-pathogenic fungi. However, we also show that these insects are less fecund and probably at no evolutionary advantage in the wild, implying that the risk is small of biological control agents failing in the field. Journal Article PLoS ONE 8 4 e60248 Insect-pathogenic fungus, Beauveria bassiana, Metarhizium anisopliae, Waxmoth, Galleria mellonella, resistance, immunity, stress response, immune priming, antimicrobial peptides, integument, fat body, biological control agent, microevolution 31 12 2013 2013-12-31 10.1371/journal.pone.0060248 COLLEGE NANME Biosciences COLLEGE CODE SBI Swansea University 2015-06-17T21:28:01.2176632 2013-04-02T09:45:50.2947202 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences François Leulier 1 Ivan M. Dubovskiy 2 Miranda M. A. Whitten 3 Olga N. Yaroslavtseva 4 Carolyn Greig 5 Vadim Y. Kryukov 6 Ekaterina V. Grizanova 7 Krishnendu Mukherjee 8 Andreas Vilcinskas 9 Viktor V. Glupov 10 Tariq Butt 0000-0002-8789-9543 11 |
| title |
Can Insects Develop Resistance to Insect Pathogenic Fungi? |
| spellingShingle |
Can Insects Develop Resistance to Insect Pathogenic Fungi? Tariq Butt |
| title_short |
Can Insects Develop Resistance to Insect Pathogenic Fungi? |
| title_full |
Can Insects Develop Resistance to Insect Pathogenic Fungi? |
| title_fullStr |
Can Insects Develop Resistance to Insect Pathogenic Fungi? |
| title_full_unstemmed |
Can Insects Develop Resistance to Insect Pathogenic Fungi? |
| title_sort |
Can Insects Develop Resistance to Insect Pathogenic Fungi? |
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85d1c2ddde272a1176e74978e25ebece |
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85d1c2ddde272a1176e74978e25ebece_***_Tariq Butt |
| author |
Tariq Butt |
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François Leulier Ivan M. Dubovskiy Miranda M. A. Whitten Olga N. Yaroslavtseva Carolyn Greig Vadim Y. Kryukov Ekaterina V. Grizanova Krishnendu Mukherjee Andreas Vilcinskas Viktor V. Glupov Tariq Butt |
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PLoS ONE |
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e60248 |
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2013 |
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Swansea University |
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10.1371/journal.pone.0060248 |
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Faculty of Science and Engineering |
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Faculty of Science and Engineering |
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School of Biosciences, Geography and Physics - Biosciences{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Biosciences, Geography and Physics - Biosciences |
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This paper presents new, important information on the microevolution of insect resistance to the insect pathogenic fungus Beauveria bassiana which will have far-reaching implications for the development of insect pathogenic fungi as biological control agents. We placed successive generations of a melanic population of the Greater wax moth, Galleria mellonella, under constant selective pressure from the insect pathogenic fungus, Beauveria bassiana. Enhanced fungal resistance was observed and larvae from the 25th generation were studied in detail to uncover mechanisms underpinning resistance, and the possible cost of those survival strategies. There are 3 novel, core findings from the study:1.Antifungal resistance in these insects is pathogen species-specific, and probably arises through trans-generational immune priming. The resistance was less obvious in earlier generations, suggesting subtle cumulative changes that are only fully apparent in the 25th generation. 2.The insect’s fecundity is already pushed close to minimum by its melanic phenotype. Therefore, the additional drain on resources required to boost antifungal defence still more, comes not from further compromising life history traits but via a re-allocation of the insect’s immune defences. Specifically during B. bassiana infection, systemic (fat body and hemocoel) responses, particularly the expression of antimicrobial peptides, are damped down in favour of a tailored repertoire of enhanced responses in the integument (cuticle and epidermis) – the foremost and most important barrier to natural fungal infection. 3.A previously-overlooked range of putative stress-management factors are activated during the specific response of selected insects to B. bassiana. This too occurs primarily in the integument, and contributes to antifungal defense and/or helps ameliorate the damage inflicted by the fungus or the host’s own immune responses during the battle between host and pathogen.No other study to date has examined so many genes in this context. Indeed, we show that the epidermis has a great capacity to express defense and stress-management genes as well as the fat body (which is the main tissue producing antimicrobial peptides and has been the traditional focus of attention). We therefore propose a “be specific / fight locally / de-stress” model to explain resource allocation and defence priorities for insects selected for superior resistance to insect-pathogenic fungi. However, we also show that these insects are less fecund and probably at no evolutionary advantage in the wild, implying that the risk is small of biological control agents failing in the field. |
| published_date |
2013-12-31T03:16:36Z |
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1763750336966688768 |
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11.035634 |