Pathogen-Mediated Alterations of Insect Chemical Communication: From Pheromones to Behavior.

Andrea Moyano, Anna Cleta Croce, Francesca Scolari
Author Information
  1. Andrea Moyano: Institute of Molecular Genetics, Italian National Research Council (CNR), Via Abbiategrasso 207, I-27100 Pavia, Italy.
  2. Anna Cleta Croce: Institute of Molecular Genetics, Italian National Research Council (CNR), Via Abbiategrasso 207, I-27100 Pavia, Italy. ORCID
  3. Francesca Scolari: Institute of Molecular Genetics, Italian National Research Council (CNR), Via Abbiategrasso 207, I-27100 Pavia, Italy. ORCID

Abstract

Pathogens can influence the physiology and behavior of both animal and plant hosts in a manner that promotes their own transmission and dispersal. Recent research focusing on insects has revealed that these manipulations can extend to the production of pheromones, which are pivotal in chemical communication. This review provides an overview of the current state of research and available data concerning the impacts of bacterial, viral, fungal, and eukaryotic pathogens on chemical communication across different insect orders. While our understanding of the influence of pathogenic bacteria on host chemical profiles is still limited, viral infections have been shown to induce behavioral changes in the host, such as altered pheromone production, olfaction, and locomotion. Entomopathogenic fungi affect host chemical communication by manipulating cuticular hydrocarbons and pheromone production, while various eukaryotic parasites have been observed to influence insect behavior by affecting the production of pheromones and other chemical cues. The effects induced by these infections are explored in the context of the evolutionary advantages they confer to the pathogen. The molecular mechanisms governing the observed pathogen-mediated behavioral changes, as well as the dynamic and mutually influential relationships between the pathogen and its host, are still poorly understood. A deeper comprehension of these mechanisms will prove invaluable in identifying novel targets in the perspective of practical applications aimed at controlling detrimental insect species.

Keywords

References

Trans R Soc Trop Med Hyg. 1973;67(5):727-8 [PMID: 4798390]
PLoS Negl Trop Dis. 2014 Apr 24;8(4):e2517 [PMID: 24762803]
Nature. 1971 Apr 16;230(5294):472-3 [PMID: 4929984]
Med Vet Entomol. 2018 Sep;32(3):358-364 [PMID: 29858503]
J Fish Dis. 2017 Mar;40(3):443-446 [PMID: 27396581]
PLoS Genet. 2019 Mar 15;15(3):e1008005 [PMID: 30875383]
Nature. 2001 Nov 29;414(6863):506 [PMID: 11734840]
Nat Prod Rep. 2015 Jul;32(7):904-36 [PMID: 25891201]
PLoS Pathog. 2006 Jun;2(6):e56 [PMID: 16789834]
Int J Dev Biol. 1998 Jan;42(1):33-42 [PMID: 9496784]
Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3376-81 [PMID: 10725405]
Arch Insect Biochem Physiol. 2000 Jun;44(2):49-68 [PMID: 10861866]
Curr Opin Immunol. 2016 Feb;38:8-17 [PMID: 26569344]
Comp Biochem Physiol A Mol Integr Physiol. 2007 Jul;147(3):711-730 [PMID: 17046303]
Physiol Behav. 2003 Aug;79(3):441-9 [PMID: 12954438]
J Fungi (Basel). 2019 Apr 16;5(2): [PMID: 31014042]
J Gen Microbiol. 1980 Sep;120(1):173-81 [PMID: 7012273]
Annu Rev Entomol. 2008;53:523-42 [PMID: 17877458]
Microbes Infect. 2006 Feb;8(2):308-15 [PMID: 16213176]
Science. 2014 Jan 17;343(6168):287-90 [PMID: 24436417]
Nat Commun. 2017 Aug 16;8(1):265 [PMID: 28814724]
Ann Microbiol (Paris). 1975 Sep;126(2):231-49 [PMID: 814853]
Proc Natl Acad Sci U S A. 2014 Jan 28;111(4):1343-8 [PMID: 24474758]
Insect Biochem Mol Biol. 2018 Nov;102:11-20 [PMID: 30243802]
J Chem Ecol. 2015 Oct;41(10):871-83 [PMID: 26410609]
PLoS Negl Trop Dis. 2008 Mar 12;2(3):e192 [PMID: 18335067]
FEBS J. 2021 Jul;288(13):3928-3947 [PMID: 33021015]
Sci Rep. 2021 Nov 5;11(1):21710 [PMID: 34741040]
Elife. 2018 Jan 09;7: [PMID: 29310753]
Prog Lipid Res. 2015 Jul;59:88-105 [PMID: 26080085]
Sci Rep. 2023 Aug 24;13(1):13821 [PMID: 37620441]
Annu Rev Entomol. 2021 Jan 7;66:45-60 [PMID: 33417824]
Biol Lett. 2011 Feb 23;7(1):67-70 [PMID: 20719770]
PLoS Pathog. 2012;8(3):e1002631 [PMID: 22479185]
J Insect Physiol. 2007 Jul;53(7):708-14 [PMID: 17509610]
Insect Biochem Mol Biol. 2023 Aug;159:103987 [PMID: 37429385]
J Invertebr Pathol. 2002 Jun;80(2):81-9 [PMID: 12383433]
Virology. 1981 Oct 15;114(1):268-72 [PMID: 18635095]
Mol Cell Proteomics. 2004 Feb;3(2):156-66 [PMID: 14645501]
Microbiol Spectr. 2017 Mar;5(2): [PMID: 28256192]
J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2010 Oct;196(10):685-700 [PMID: 20680632]
J Parasitol. 1996 Dec;82(6):1037-9 [PMID: 8973421]
EMBO Rep. 2009 Mar;10(3):212-5 [PMID: 19255576]
J Invertebr Pathol. 2000 Feb;75(2):144-51 [PMID: 10772327]
Science. 2010 Nov 19;330(6007):1102-4 [PMID: 21097935]
J Invertebr Pathol. 1991 Jul;58(1):82-7 [PMID: 1885925]
Annu Rev Microbiol. 2013;67:271-89 [PMID: 23808340]
Science. 1997 Jun 6;276(5318):1555-8 [PMID: 9171057]
Microb Ecol. 2015 May;69(4):723-32 [PMID: 25117532]
PLoS Negl Trop Dis. 2014 Apr 24;8(4):e2645 [PMID: 24763082]
J Exp Biol. 2019 Jul 17;222(Pt 14): [PMID: 31315924]
Medicina (B Aires). 1980;40 Suppl 1:178-80 [PMID: 7005600]
Behav Ecol Sociobiol. 2014;68(12):2059-2073 [PMID: 25395721]
Proc Natl Acad Sci U S A. 2005 Feb 15;102(7):2584-9 [PMID: 15699333]
Front Plant Sci. 2016 Jun 23;7:885 [PMID: 27446117]
Insects. 2021 Apr 30;12(5): [PMID: 33946603]
Arch Biochem Biophys. 1997 Aug 1;344(1):208-14 [PMID: 9244399]
Proc Natl Acad Sci U S A. 2002 May 14;99(10):6838-42 [PMID: 12011442]
PLoS Pathog. 2021 Sep 16;17(9):e1009539 [PMID: 34529715]
Proc Natl Acad Sci U S A. 2015 Dec 22;112(51):15678-83 [PMID: 26644557]
PLoS Pathog. 2013;9(6):e1003372 [PMID: 23785277]
Microb Biotechnol. 2017 May;10(3):531-540 [PMID: 27943632]
mBio. 2015 Mar 24;6(2): [PMID: 25805727]
Annu Rev Entomol. 2016;61:239-56 [PMID: 26667271]
Viruses. 2020 Jan 25;12(2): [PMID: 31991772]
J Chem Ecol. 2009 Dec;35(12):1437-47 [PMID: 20063206]
PLoS One. 2012;7(12):e50679 [PMID: 23272066]
Nature. 2007 Jan 18;445(7125):275-80 [PMID: 17136098]
Adv Genet. 2016;94:437-69 [PMID: 27131331]
BMC Microbiol. 2018 Nov 23;18(Suppl 1):169 [PMID: 30470198]
Science. 1971 Oct 1;174(4004):76-8 [PMID: 5120874]
Parasitology. 1980 Oct;81(2):405-21 [PMID: 7443302]
Annu Rev Entomol. 2005;50:371-93 [PMID: 15355247]
Lab Anim (NY). 2018 Jun;47(6):157-164 [PMID: 29795158]
Cell Host Microbe. 2010 Feb 18;7(2):164-75 [PMID: 20159621]
J Chem Ecol. 2006 Sep;32(9):2035-52 [PMID: 16902820]
Genetika. 2007 Sep;43(9):1277-80 [PMID: 17990528]
Adv Genet. 2016;94:251-85 [PMID: 27131327]
Int J Mol Sci. 2021 Mar 30;22(7): [PMID: 33808210]
Cell Host Microbe. 2009 Feb 19;5(2):200-11 [PMID: 19218090]
J Insect Physiol. 2006 Nov-Dec;52(11-12):1128-36 [PMID: 17046784]
Proc Natl Acad Sci U S A. 2012 Jan 3;109(1):249-54 [PMID: 22114190]
Front Microbiol. 2013 Feb 15;4:24 [PMID: 23422735]
J Invertebr Pathol. 2013 May;113(1):42-51 [PMID: 23352958]
Parasite Immunol. 2015 Mar;37(3):159-70 [PMID: 25376390]
R Soc Open Sci. 2021 Apr 28;8(4):210194 [PMID: 34007462]
Results Probl Cell Differ. 2020;69:497-536 [PMID: 33263885]
Proc Natl Acad Sci U S A. 2012 Sep 11;109(37):14858-63 [PMID: 22927409]
Parasitology. 1986 Aug;93 ( Pt 1):111-20 [PMID: 3748608]
Int J Mol Sci. 2019 Sep 17;20(18): [PMID: 31533250]
PLoS Genet. 2023 Jun 15;19(6):e1010782 [PMID: 37319172]
Eur J Biochem. 2003 Aug;270(16):3398-407 [PMID: 12899697]
Mol Ecol. 2007 Nov;16(22):4837-48 [PMID: 17927707]
Trends Ecol Evol. 2006 May;21(5):278-86 [PMID: 16697914]
Nat Prod Rep. 2018 May 25;35(5):386-397 [PMID: 29565067]
Front Cell Infect Microbiol. 2020 Jun 23;10:214 [PMID: 32656090]
Commun Biol. 2021 Jul 26;4(1):911 [PMID: 34312484]
J Invertebr Pathol. 2002 Sep;81(1):33-44 [PMID: 12417211]
Annu Rev Entomol. 2010;55:247-66 [PMID: 19728837]
J Invertebr Pathol. 1987 May;49(3):227-34 [PMID: 3585048]
J Insect Physiol. 2019 Oct;118:103918 [PMID: 31400384]
J Chem Ecol. 2010 May;36(5):522-5 [PMID: 20401523]
J Insect Physiol. 2014 Dec;71:122-7 [PMID: 25450424]
Insects. 2020 Sep 23;11(10): [PMID: 32977418]
Oecologia. 1988 May;75(4):516-520 [PMID: 28312425]
Proc Natl Acad Sci U S A. 1995 May 23;92(11):5082-6 [PMID: 7761452]
Mol Ecol. 2018 Sep;27(18):3582-3598 [PMID: 30052297]
J Invertebr Pathol. 2004 Feb;85(2):128-31 [PMID: 15050843]
PLoS One. 2013 Sep 18;8(9):e75246 [PMID: 24058668]
Sci Rep. 2016 Feb 05;6:20334 [PMID: 26847001]
Annu Rev Entomol. 2009;54:189-207 [PMID: 19067631]
Science. 2007 Jul 20;317(5836):384-6 [PMID: 17641204]
J Exp Biol. 2009 May;212(Pt 10):1436-41 [PMID: 19411536]
Parasitol Res. 2009 Sep;105(3):875-9 [PMID: 19471965]
J Invertebr Pathol. 1971 Nov;18(3):373-7 [PMID: 5151912]
Ecol Evol. 2023 Oct 14;13(10):e10627 [PMID: 37841224]
Res Microbiol. 2002 Oct;153(8):503-9 [PMID: 12437211]
PLoS Pathog. 2012;8(3):e1002610 [PMID: 22457628]
Mol Ecol. 2014 Dec;23(24):6114-22 [PMID: 25142402]
J Anim Ecol. 2022 Jan;91(1):101-111 [PMID: 34626485]
Front Insect Sci. 2022 Mar 17;2:859847 [PMID: 38468774]
Curr Opin Insect Sci. 2014 Oct;4:1-7 [PMID: 28043402]
G3 (Bethesda). 2020 Jul 7;10(7):2275-2296 [PMID: 32354705]
Nat Rev Immunol. 2014 Dec;14(12):796-810 [PMID: 25421701]
PLoS Negl Trop Dis. 2020 Sep 10;14(9):e0008531 [PMID: 32911504]
Insects. 2021 Mar 26;12(4): [PMID: 33810245]
Insect Biochem Mol Biol. 2019 Jul;110:52-59 [PMID: 31051237]
mSphere. 2020 Apr 15;5(2): [PMID: 32295874]
Pathogens. 2023 Apr 05;12(4): [PMID: 37111444]
Insects. 2022 Oct 31;13(11): [PMID: 36354821]
Am Nat. 2009 Sep;174(3):424-33 [PMID: 19627240]
Insect Mol Biol. 2018 Oct;27(5):661-674 [PMID: 29896786]
Sci Rep. 2021 May 27;11(1):11258 [PMID: 34045618]
Proc Biol Sci. 2020 Sep 30;287(1935):20201303 [PMID: 32962544]
J Chem Ecol. 2010 Apr;36(4):441-8 [PMID: 20349337]
Naturwissenschaften. 2003 Oct;90(10):477-80 [PMID: 14564409]
J Chem Ecol. 2013 Jul;39(7):840-59 [PMID: 23793954]
Science. 2005 Dec 16;310(5755):1781 [PMID: 16357252]
Proc Biol Sci. 2000 Aug 7;267(1452):1591-4 [PMID: 11007336]
J Insect Sci. 2005;5:6 [PMID: 16299596]
Genetica. 2002 Apr;114(3):269-74 [PMID: 12206365]
Annu Rev Entomol. 2015 Jan 7;60:351-71 [PMID: 25341093]
Proc Natl Acad Sci U S A. 2005 Aug 9;102(32):11414-9 [PMID: 16061818]
Sci Rep. 2023 Sep 1;13(1):14363 [PMID: 37658067]
J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2003 Sep;189(9):675-84 [PMID: 12879351]
Annu Rev Entomol. 2014;59:467-85 [PMID: 24160418]
Proc Natl Acad Sci U S A. 2007 Apr 10;104(15):6442-7 [PMID: 17404235]
J Invertebr Pathol. 2020 Jul;174:107398 [PMID: 32473941]
PLoS Negl Trop Dis. 2012;6(10):e1859 [PMID: 23145192]
Annu Rev Entomol. 2014;59:405-25 [PMID: 24397521]
J Med Entomol. 2002 May;39(3):545-52 [PMID: 12061454]
Heredity (Edinb). 2021 Feb;126(2):219-234 [PMID: 33139902]
J Parasitol. 2003 Jun;89(3):516-21 [PMID: 12880251]
Elife. 2019 Sep 11;8: [PMID: 31509107]
Biol Lett. 2019 Nov 29;15(11):20190557 [PMID: 31744410]
Bioessays. 2015 Jul;37(7):822-30 [PMID: 25988392]
Proc Biol Sci. 2019 Jun 26;286(1905):20190517 [PMID: 31213188]
J Exp Biol. 2002 Mar;205(Pt 6):781-90 [PMID: 11914386]
ISME J. 2022 Oct;16(10):2388-2397 [PMID: 35831484]
Proc Natl Acad Sci U S A. 2016 Aug 16;113(33):9268-73 [PMID: 27439866]
J Invertebr Pathol. 2011 Mar;106(3):380-5 [PMID: 21156180]
Insect Biochem Mol Biol. 2021 Nov;138:103648 [PMID: 34536505]
BMC Biol. 2021 Sep 23;19(1):211 [PMID: 34556101]
J Chem Ecol. 2007 Nov;33(11):2167-70 [PMID: 17940824]
Curr Opin Insect Sci. 2015 Jun;9:16-23 [PMID: 32846703]
Front Microbiol. 2022 May 03;13:870462 [PMID: 35591988]
J Invertebr Pathol. 2000 Jul;76(1):6-12 [PMID: 10963397]
J Insect Physiol. 2009 Jan;55(1):59-69 [PMID: 19013465]
PLoS Pathog. 2022 Apr 4;18(4):e1010442 [PMID: 35377922]
Ecol Lett. 2021 Oct;24(10):2113-2122 [PMID: 34265869]
Nature. 2023 Jan;613(7943):324-331 [PMID: 36599989]
Science. 2023 Feb 17;379(6633):eade1877 [PMID: 36795837]
BMC Genomics. 2015 Aug 19;16:620 [PMID: 26285697]
Ecol Lett. 2013 Apr;16(4):493-501 [PMID: 23351125]
Proc Natl Acad Sci U S A. 2010 Nov 16;107(46):20051-6 [PMID: 21041648]

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