1932

Abstract

Parasite manipulation of host behavior, as an effective strategy to establish transmission, has evolved multiple times across taxa, including fungi. Major strides have been made to propose molecular mechanisms that underlie manipulative parasite-host interactions including the manipulation of carpenter ant behavior by . This research suggests that the secretion of parasite proteins and light-driven biological rhythms are likely involved in the infection and manipulation biology of and other manipulating parasites. Here, we discuss research on considering findings from other (fungal) parasites that either are relatively closely related (e.g., other insect- and plant-infecting Hypocreales) or also manipulate insect behavior (e.g., Entomophthorales). As such, this review aims to put forward this question: Are the mechanisms behind manipulation and infection unique, or did they convergently evolve? From this discussion, we pose functional hypotheses about the infection biology of that will need to be addressed in future studies.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-041522-092522
2024-11-20
2025-02-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/78/1/annurev-micro-041522-092522.html?itemId=/content/journals/10.1146/annurev-micro-041522-092522&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Adamo SA, Linn CE, Beckage NE. 1997.. Correlation between changes in host behaviour and octopamine levels in the tobacco hornworm Manduca sexta parasitized by the gregarious braconid parasitoid wasp Cotesia congregata. . J. Exp. Biol. 200::11727
    [Crossref] [Google Scholar]
  2. 2.
    Andriolli FS, Ishikawa NK, Vargas-Isla R, Cabral TS, de Bekker C, Baccaro FB. 2019.. Do zombie ant fungi turn their hosts into light seekers?. Behav. Ecol. 30::60916
    [Crossref] [Google Scholar]
  3. 3.
    Araújo JPM, Evans HC, Fernandes IO, Ishler MJ, Hughes DP. 2020.. Zombie-ant fungi cross continents: II. Myrmecophilous hymenostilboid species and a novel zombie lineage. . Mycologia 112::113870
    [Crossref] [Google Scholar]
  4. 4.
    Araújo JPM, Evans HC, Geiser DM, Mackay WP, Hughes DP. 2015.. Unravelling the diversity behind the Ophiocordyceps unilateralis (Ophiocordycipitaceae) complex: three new species of zombie-ant fungi from the Brazilian Amazon. . Phytotaxa 220::22438
    [Crossref] [Google Scholar]
  5. 5.
    Araújo JPM, Evans HC, Kepler R, Hughes DP. 2018.. Zombie-ant fungi across continents: 15 new species and new combinations within Ophiocordyceps. I. Myrmecophilous hirsutelloid species. . Stud. Mycol. 90::11960
    [Crossref] [Google Scholar]
  6. 6.
    Araújo JPM, Hughes DP. 2016.. Diversity of entomopathogenic fungi: Which groups conquered the insect body?. Adv. Genet. 94::139
    [Crossref] [Google Scholar]
  7. 7.
    Araújo JPM, Hughes DP. 2017.. The fungal spore: myrmecophilous Ophiocordyceps as a case study. . In The Fungal Community: Its Organization and Role in the Ecosystem, ed. J Dighton, JF White , pp. 35967. Boca Raton, FL:: CRC Press. , 4th ed..
    [Google Scholar]
  8. 8.
    Araújo JPM, Hughes DP. 2019.. Zombie-ant fungi emerged from non-manipulating, beetle-infecting ancestors. . Curr. Biol. 29::373538.e2
    [Crossref] [Google Scholar]
  9. 9.
    Barbosa BC, Maciela TT, Paschoalini M, Prezoto F. 2016.. Entomopathogenic fungi in Diptera: remarks on range extension and collection records. . Bol. Mus. Biol. Mello Leitão 38::25763
    [Google Scholar]
  10. 10.
    Beckerson WC, Krider C, Mohammad UA, de Bekker C. 2023.. 28 minutes later: investigating the role of aflatrem-like compounds in Ophiocordyceps parasite manipulation of zombie ants. . Anim. Behav. 203::22540
    [Crossref] [Google Scholar]
  11. 11.
    Ben-Shahar Y, Leung H, Pak W, Sokolowski M, Robinson G. 2003.. cGMP-dependent changes in phototaxis: a possible role for the foraging gene in honey bee division of labor. . J. Exp. Biol. 206::250715
    [Crossref] [Google Scholar]
  12. 12.
    Berisford Y, Tsao C. 1974.. Field and laboratory observations of an entomogenous infection of the adult seedcorn maggot, Hylemya platura (Diptera: Anthomyiidae). . J. Ga. Entomol. Soc. 9:(2):10410
    [Google Scholar]
  13. 13.
    Bhattarai UR, Li F, Katuwal Bhattarai M, Masoudi A, Wang D. 2018.. Phototransduction and circadian entrainment are the key pathways in the signaling mechanism for the baculovirus induced tree-top disease in the lepidopteran larvae. . Sci. Rep. 8::17528
    [Crossref] [Google Scholar]
  14. 14.
    Biernat MA, Eker AP, van Oers MM, Vlak JM, van der Horst GT, Chaves I. 2012.. A baculovirus photolyase with DNA repair activity and circadian clock regulatory function. . J. Biol. Rhythms 27::311
    [Crossref] [Google Scholar]
  15. 15.
    Camp JW, Huizinga HW. 1979.. Altered color, behavior and predation susceptibility of the isopod Asellus intermedius infected with Acanthocephalus dirus. . J. Parasitol. 65::66769
    [Crossref] [Google Scholar]
  16. 16.
    Ceriani MF, Hogenesch JB, Yanovsky M, Panda S, Straume M, Kay SA. 2002.. Genome-wide expression analysis in Drosophila reveals genes controlling circadian behavior. . J. Neurosci. 22::930519
    [Crossref] [Google Scholar]
  17. 17.
    Cha J, Zhou M, Liu Y. 2015.. Mechanism of the Neurospora circadian clock, a FREQUENCY-centric view. . Biochemistry 54::15056
    [Crossref] [Google Scholar]
  18. 18.
    Chung TY, Sun PF, Kuo JI, Lee YI, Lin CC, Chou JY. 2017.. Zombie ant heads are oriented relative to solar cues. . Fungal Ecol. 25::2228
    [Crossref] [Google Scholar]
  19. 19.
    Cole RJ. 1981.. Fungal tremorgens. . J. Food Prot. 44::71522
    [Crossref] [Google Scholar]
  20. 20.
    Das B, Brachmann A, de Bekker C. 2023.. Both behavior-manipulating and non-manipulating entomopathogenic fungi affect rhythmic gene expression in carpenter ant foragers upon infection. . bioRxiv 2023.01.19.524837. https://doi.org/10.1101/2023.01.19.524837
  21. 21.
    Das B, de Bekker C. 2022.. Time-course RNASeq of Camponotus floridanus forager and nurse ant brains indicate links between plasticity in the biological clock and behavioral division of labor. . BMC Genom. 23::57
    [Crossref] [Google Scholar]
  22. 22.
    Das B, Will I, Brouns R, Brachmann A, de Bekker C. 2023.. Using RNASeq to investigate the involvement of the Ophiocordyceps clock in ant host infection and behavioral manipulation. . bioRxiv 2023.01.20.524843. https://doi.org/10.1101/2023.01.20.524843
  23. 23.
    Dawkins R. 1982.. The Extended Phenotype: The Gene as the Unit of Selection. New York:: Oxford Univ. Press
    [Google Scholar]
  24. 24.
    Dawkins R. 1990.. Parasites, desiderata lists and the paradox of the organism. . Parasitology 100::S6373
    [Crossref] [Google Scholar]
  25. 25.
    Dawkins R. 2004.. Extended phenotype—but not too extended. A reply to Laland, Turner and Jablonka. . Biol. Philos. 19::37796
    [Crossref] [Google Scholar]
  26. 26.
    de Bekker C, Beckerson W, Elya C. 2021.. Mechanisms behind the madness: How do zombie-making fungal entomopathogens affect host behavior to increase transmission?. mBio 12::e01872-21
    [Crossref] [Google Scholar]
  27. 27.
    de Bekker C, Das B. 2022.. Hijacking time: how Ophiocordyceps fungi could be using ant host clocks to manipulate behavior. . Parasite Immunol. 44::e12909
    [Crossref] [Google Scholar]
  28. 28.
    de Bekker C, Ohm RA, Evans HC, Brachmann A, Hughes DP. 2017.. Ant-infecting Ophiocordyceps genomes reveal a high diversity of potential behavioral manipulation genes and a possible major role for enterotoxins. . Sci. Rep. 7::12508
    [Crossref] [Google Scholar]
  29. 29.
    de Bekker C, Ohm RA, Loreto RG, Sebastian A, Albert I, et al. 2015.. Gene expression during zombie ant biting behavior reflects the complexity underlying fungal parasitic behavioral manipulation. . BMC Genom. 16::620
    [Crossref] [Google Scholar]
  30. 30.
    de Bekker C, Smith PB, Patterson AD, Hughes DP. 2014.. Metabolomics reveals the heterogeneous secretome of two entomopathogenic fungi to ex vivo cultured insect tissues. . PLOS ONE 8::e70609
    [Crossref] [Google Scholar]
  31. 31.
    de Bekker C, Will I, Hughes DP, Brachmann A, Merrow M. 2017.. Daily rhythms and enrichment patterns in the transcriptome of the behavior-manipulating parasite Ophiocordyceps kimflemingiae. . PLOS ONE 12::e0187170
    [Crossref] [Google Scholar]
  32. 32.
    Ding JL, Wei K, Feng MG, Ying SH. 2023.. Homologs of bacterial heat-labile enterotoxin subunit A contribute to development, stress response, and virulence in filamentous entomopathogenic fungus Beauveria bassiana. . Front. Immunol. 14::1264560
    [Crossref] [Google Scholar]
  33. 33.
    Eberhard WG. 2000.. Spider manipulation by a wasp larva. . Nature 406::25556
    [Crossref] [Google Scholar]
  34. 34.
    Elya C, Lavrentovich D, Lee E, Pasadyn C, Duval J, et al. 2023.. Neural mechanisms of parasite-induced summiting behavior in ‘zombie’ Drosophila. . eLife 12::e85410
    [Crossref] [Google Scholar]
  35. 35.
    Elya C, Lok TC, Spencer QE, McCausland H, Martinez CC, Eisen M. 2018.. Robust manipulation of the behavior of Drosophila melanogaster by a fungal pathogen in the laboratory. . eLife 7::e34414
    [Crossref] [Google Scholar]
  36. 36.
    Evans HC, Elliot SL, Hughes DP. 2011.. Hidden diversity behind the zombie-ant fungus Ophiocordyceps unilateralis: four new species described from carpenter ants in Minas Gerais, Brazil. . PLOS ONE 6::e17024
    [Crossref] [Google Scholar]
  37. 37.
    Evans HC, Elliot SL, Hughes DP. 2011.. Ophiocordyceps unilateralis: a keystone species for unraveling ecosystem functioning and biodiversity of fungi in tropical forests?. Commun. Integr. Biol. 4::598602
    [Crossref] [Google Scholar]
  38. 38.
    Fitzpatrick MJ, Sokolowski MB. 2004.. In search of food: exploring the evolutionary link between cGMP-dependent protein kinase (PKG) and behaviour. . Integr. Comp. Biol. 44::2836
    [Crossref] [Google Scholar]
  39. 39.
    Franks NR, Tofts C. 1994.. Foraging for work: how tasks allocate workers. . Anim. Behav. 48::47072
    [Crossref] [Google Scholar]
  40. 40.
    Fredericksen MA, Zhang Y, Hazen ML, Loreto RG, Mangold CA, et al. 2017.. Three-dimensional visualization and a deep-learning model reveal complex fungal parasite networks in behaviorally manipulated ants. . PNAS 114::1259095
    [Crossref] [Google Scholar]
  41. 41.
    Fujioka H, Abe MS, Fuchikawa T, Tsuji K, Shimada M, Okada Y. 2017.. Ant circadian activity associated with brood care type. . Biol. Lett. 13::20160743
    [Crossref] [Google Scholar]
  42. 42.
    Gasque SN, Fredensborg BL. 2023.. Expression of trematode-induced zombie-ant behavior is strongly associated with temperature. . Behav. Ecol. 34:(6):96068
    [Crossref] [Google Scholar]
  43. 43.
    Goulson D. 1997.. Wipfelkrankheit: modification of host behaviour during baculoviral infection. . Oecologia 109::21928
    [Crossref] [Google Scholar]
  44. 44.
    Han Y, van Houte S, van Oers MM, VID Ros. 2018.. Timely trigger of caterpillar zombie behaviour: temporal requirements for light in baculovirus-induced tree-top disease. . Parasitology 145::82227
    [Crossref] [Google Scholar]
  45. 45.
    Henrik H, Edwards S, Elya C, Henrik H. 2023.. Evolutionary ecology of an obligate and behaviorally manipulating insect-pathogenic fungus, Entomophthora muscae. . Authorea 2023:. https://doi.org/10.22541/au.167778641.14505987/v1
    [Google Scholar]
  46. 46.
    Herbison REH. 2017.. Lessons in mind control: trends in research on the molecular mechanisms behind parasite-host behavioral manipulation. . Front. Ecol. Evol. 5::102
    [Crossref] [Google Scholar]
  47. 47.
    Hevia MA, Canessa P, Müller-Esparza H, Larrondo LF. 2015.. A circadian oscillator in the fungus Botrytis cinerea regulates virulence when infecting Arabidopsis thaliana. . PNAS 112::874449
    [Crossref] [Google Scholar]
  48. 48.
    Hofmann R. 1891.. Insektentötende Pilze mit besonderer Berücksichtigung der “Nonne.” Frankfurt, Ger:.: P. Weber
    [Google Scholar]
  49. 49.
    Hughes DP, Andersen SB, Hywel-Jones NL, Himaman W, Billen J, Boomsma JJ. 2011.. Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. . BMC Ecol. 11::13
    [Crossref] [Google Scholar]
  50. 50.
    Hughes DP, Araújo JP, Loreto RG, Quevillon L, de Bekker C, Evans HC. 2016.. From so simple a beginning: the evolution of behavioral manipulation by fungi. . Adv. Genet. 94::43769
    [Crossref] [Google Scholar]
  51. 51.
    Hughes DP, Wappler T, Labandeira CC. 2011.. Ancient death-grip leaf scars reveal ant–fungal parasitism. . Biol. Lett. 7::6770
    [Crossref] [Google Scholar]
  52. 52.
    Ibrahim AM, Kim Y. 2008.. Transient expression of protein tyrosine phosphatases encoded in Cotesia plutellae bracovirus inhibits insect cellular immune responses. . Naturwissenschaften 95::2532
    [Crossref] [Google Scholar]
  53. 53.
    Ingram KK, Kleeman L, Peteru S. 2011.. Differential regulation of the foraging gene associated with task behaviors in harvester ants. . BMC Ecol. 11::19
    [Crossref] [Google Scholar]
  54. 54.
    Ingwell LL, Eigenbrode SD, Bosque-Perez NA. 2012.. Plant viruses alter insect behavior to enhance their spread. . Sci. Rep. 2::578
    [Crossref] [Google Scholar]
  55. 55.
    Kamita SG, Nagasaka K, Chua JW, Shimada T, Mita K, et al. 2005.. A baculovirus-encoded protein tyrosine phosphatase gene induces enhanced locomotory activity in a lepidopteran host. . PNAS 102::258489
    [Crossref] [Google Scholar]
  56. 56.
    Katsuma S. 2015.. Phosphatase activity of Bombyx mori nucleopolyhedrovirus PTP is dispensable for enhanced locomotory activity in B. mori larvae. . J. Invert. Pathol. 132::22832
    [Crossref] [Google Scholar]
  57. 57.
    Kepler RM, Kaitsu Y, Tanaka E, Shimano S, Spatafora JW. 2011.. Ophiocordyceps pulvinata sp. nov., a pathogen with a reduced stroma. . Mycoscience 52::3947
    [Crossref] [Google Scholar]
  58. 58.
    Kim KT, Jeon J, Choi J, Cheong K, Song H, et al. 2016.. Kingdom-wide analysis of fungal small secreted proteins (SSPs) reveals their potential role in host association. . Front. Plant Sci. 7::186
    [Google Scholar]
  59. 59.
    Kobmoo N, Mongkolsamrit S, Tasanathai K, Thanakitpipattana D, Luangsa-Ard JJ. 2012.. Molecular phylogenies reveal host-specific divergence of Ophiocordyceps unilateralis sensu lato following its host ants. . Mol. Ecol. 21::302231
    [Crossref] [Google Scholar]
  60. 60.
    Kobmoo N, Mongkolsamrit S, Wutikhun T, Tasanathai K, Khonsanit A, et al. 2015.. New species of Ophiocordyceps unilateralis, an ubiquitous pathogen of ants from Thailand. . Fungal Biol. 119::4452
    [Crossref] [Google Scholar]
  61. 61.
    Kobmoo N, Wichadakul D, Arnamnart N, Rodriguez De La Vega RC, Luangsa-Ard JJ, Giraud T. 2018.. A genome scan of diversifying selection in Ophiocordyceps zombie-ant fungi suggests a role for enterotoxins in co-evolution and host specificity. . Mol. Ecol. 27::358298
    [Crossref] [Google Scholar]
  62. 62.
    Krasnoff S, Watson D, Gibson D, Kwan E. 1995.. Behavioral effects of the entomopathogenic fungus, Entomophthora muscae on its host Musca domestica: postural changes in dying hosts and gated pattern of mortality. . J. Insect Physiol. 41::895903
    [Crossref] [Google Scholar]
  63. 63.
    Krittika S, Yadav P. 2020.. Circadian clocks: an overview on its adaptive significance. . Biol. Rhythm Res. 51::110932
    [Crossref] [Google Scholar]
  64. 64.
    Kuhnert E, Collemare J. 2022.. A genomic journey in the secondary metabolite diversity of fungal plant and insect pathogens: from functional to population genomics. . Curr. Opin. Microbiol. 69::102178
    [Crossref] [Google Scholar]
  65. 65.
    Lavery MN, Murphy CFH, Bowman EK. 2021.. Zombie ant graveyard dynamics in Gunung Mulu National Park. . Reinvention 14:. https://doi.org/10.31273/reinvention.v14i1.704
    [Crossref] [Google Scholar]
  66. 66.
    Lebrigand K, He LD, Thakur N, Arguel MJ, Polanowska J, et al. 2016.. Comparative genomic analysis of Drechmeria coniospora reveals core and specific genetic requirements for fungal endoparasitism of nematodes. . PLOS Genet. 12::e1006017
    [Crossref] [Google Scholar]
  67. 67.
    Leung TL. 2017.. Fossils of parasites: What can the fossil record tell us about the evolution of parasitism?. Biol. Rev. Camb. Philos. Soc. 92::41030
    [Crossref] [Google Scholar]
  68. 68.
    Li Y, Hoffmann J, Li Y, Stephano F, Bruchhaus I, et al. 2016.. Octopamine controls starvation resistance, life span and metabolic traits in Drosophila. . Sci. Rep. 6::35359
    [Crossref] [Google Scholar]
  69. 69.
    Lima-Camara TN, Bruno RV, Luz PM, Castro MG, Lourenco-de-Oliveira R, et al. 2011.. Dengue infection increases the locomotor activity of Aedes aegypti females. . PLOS ONE 6::e17690
    [Crossref] [Google Scholar]
  70. 70.
    Liu X, Tian Z, Cai L, Shen Z, Michaud J, et al. 2022.. Baculoviruses hijack the visual perception of their caterpillar hosts to induce climbing behaviour thus promoting virus dispersal. . Mol. Ecol. 31::275265
    [Crossref] [Google Scholar]
  71. 71.
    Lone SR, Sharma VK. 2011.. Timekeeping through social contacts: social synchronization of circadian locomotor activity rhythm in the carpenter ant Camponotus paria. . Chronobiol. Int. 28::86272
    [Crossref] [Google Scholar]
  72. 72.
    Loreto RG, Araújo JP, Kepler RM, Fleming KR, Moreau CS, Hughes DP. 2018.. Evidence for convergent evolution of host parasitic manipulation in response to environmental conditions. . Evolution 72::214455
    [Crossref] [Google Scholar]
  73. 73.
    Loreto RG, Hughes DP. 2019.. The metabolic alteration and apparent preservation of the zombie ant brain. . J. Insect Phys. 118::103918
    [Crossref] [Google Scholar]
  74. 74.
    Luangsa-Ard JJ, Ridkaew R, Tasanathai K, Thanakitpipattana D, Hywel-Jones N. 2011.. Ophiocordyceps halabalaensis: a new species of Ophiocordyceps pathogenic to Camponotus gigas in Hala Bala Wildlife Sanctuary, Southern Thailand. . Fungal Biol. 115::60814
    [Crossref] [Google Scholar]
  75. 75.
    Macheleidt J, Mattern DJ, Fischer J, Netzker T, Weber J, et al. 2016.. Regulation and role of fungal secondary metabolites. . Annu. Rev. Genet. 50::37192
    [Crossref] [Google Scholar]
  76. 76.
    Maitland DP. 1994.. A parasitic fungus infecting yellow dungflies manipulates host perching behaviour. . Biol. Sci. 258::18793
    [Crossref] [Google Scholar]
  77. 77.
    Manga-González MY, González-Lanza C, Cabanas E, Campo R. 2001.. Contributions to and review of dicrocoeliosis, with special reference to the intermediate hosts of Dicrocoelium dendriticum. . Parasitology 123::91114
    [Crossref] [Google Scholar]
  78. 78.
    Manger P, Li J, Christensen BM, Yoshino TP. 1996.. Biogenic monoamines in the freshwater snail, Biomphalaria glabrata: influence of infection by the human blood fluke, Schistosoma mansoni. . Comp. Biochem. Physiol. A 114::22734
    [Crossref] [Google Scholar]
  79. 79.
    Mangold CA, Ishler MJ, Loreto RG, Hazen ML, Hughes DP. 2019.. Zombie ant death grip due to hypercontracted mandibular muscles. . J. Exp. Biol. 222::jeb200683
    [Crossref] [Google Scholar]
  80. 80.
    Meunier N, Belgacem YH, Martin JR. 2007.. Regulation of feeding behaviour and locomotor activity by takeout in Drosophila. . J. Exp. Biol. 210::142434
    [Crossref] [Google Scholar]
  81. 81.
    Mildner S, Roces F. 2017.. Plasticity of daily behavioral rhythms in foragers and nurses of the ant Camponotus rufipes: influence of social context and feeding times. . PLOS ONE 12::e0169244
    [Crossref] [Google Scholar]
  82. 82.
    Minter D, Brady B. 1980.. Mononematous species of Hirsutella. . Trans. Brit. Mycol. Soc. 74::27182
    [Crossref] [Google Scholar]
  83. 83.
    Mongkolsamrit S, Noisripoom W, Hasin S, Sinchu P, Jangsantear P, Luangsa-Ard JJ. 2023.. Multi-gene phylogeny and morphology of Ophiocordyceps laotii sp. nov. and a new record of O. buquetii (Ophiocordycipitaceae, Hypocreales) on ants from Thailand. . Mycol. Prog. 22::5
    [Crossref] [Google Scholar]
  84. 84.
    Montenegro-Montero A, Canessa P, Larrondo LF. 2015.. Around the fungal clock: recent advances in the molecular study of circadian clocks in Neurospora and other fungi. . Adv. Genet. 92::10784
    [Crossref] [Google Scholar]
  85. 85.
    Moore J. 2002.. Parasites and the Behavior of Animals. Oxford, UK:: Oxford Univ. Press
    [Google Scholar]
  86. 86.
    Neto JAC, Leal LC, Baccaro FB. 2019.. Temporal and spatial gradients of humidity shape the occurrence and the behavioral manipulation of ants infected by entomopathogenic fungi in Central Amazon. . Fungal Ecol. 42::100871
    [Crossref] [Google Scholar]
  87. 87.
    O'Reilly DR, Miller LK. 1991.. Improvement of a baculovirus pesticide by deletion of the egt gene. . Bio/Technology 9::108689
    [Crossref] [Google Scholar]
  88. 88.
    Patouillard N. 1892.. Une Clavariée eutinigène. . Rev. Mycol. 14::6770
    [Google Scholar]
  89. 89.
    Ponton F, Lefèvre T, Lebarbenchon C, Thomas F, Loxdale H, et al. 2006.. Do distantly related parasites rely on the same proximate factors to alter the behaviour of their hosts?. Proc. R. Soc. B 273::286977
    [Crossref] [Google Scholar]
  90. 90.
    Ponton F, Otálora-Luna F, Lefevre T, Guerin PM, Lebarbenchon C, et al. 2011.. Water-seeking behavior in worm-infected crickets and reversibility of parasitic manipulation. . Behav. Ecol. 22::392400
    [Crossref] [Google Scholar]
  91. 91.
    Poulin R. 1994.. The evolution of parasite manipulation of host behaviour: a theoretical analysis. . Parasitology 109::S10918
    [Crossref] [Google Scholar]
  92. 92.
    Robert V, Vu D, Amor ABH, van de Wiele N, Brouwer C, et al. 2013.. MycoBank gearing up for new horizons. . IMA Fungus 4::37179
    [Crossref] [Google Scholar]
  93. 93.
    Roeder T. 2005.. Tyramine and octopamine: ruling behavior and metabolism. . Annu. Rev. Entomol. 50::44777
    [Crossref] [Google Scholar]
  94. 94.
    Rosbash M. 2009.. The implications of multiple circadian clock origins. . PLOS Biol. 7::e1000062
    [Crossref] [Google Scholar]
  95. 95.
    Sharma A, Kaur E, Joshi R, Kumari P, Khatri A, et al. 2023.. Systematic analyses with genomic and metabolomic insights reveal a new species, Ophiocordyceps indica sp. nov. from treeline area of Indian Western Himalayan region. . Front. Microbiol. 14::1188649
    [Crossref] [Google Scholar]
  96. 96.
    Sobczak JF, Arruda IDP, Fonseca EO, Queiroz Rabelo PJ, de Sousa Nóbrega FA, et al. 2020.. Manipulation of wasp (Hymenoptera: Vespidae) behavior by the entomopathogenic fungus Ophiocordyceps humbertii in the Atlantic forest in Ceará, Brazil. . Entomol. News 129::98104
    [Crossref] [Google Scholar]
  97. 97.
    Spangler BD. 1992.. Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. . Microbiol. Rev. 56::62247
    [Crossref] [Google Scholar]
  98. 98.
    Stajich JE, Lovett B, Lee E, Macias AM, Hajek AE, et al. 2024.. Signatures of transposon-mediated genome inflation, host specialization, and photoentrainment in Entomophthora muscae and allied entomophthoralean fungi. . eLife 12::RP92863
    [Crossref] [Google Scholar]
  99. 99.
    Sung GH, Hywel-Jones NL, Sung JM, Luangsa-Ard JJ, Shrestha B, Spatafora JW. 2007.. Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. . Stud. Mycol. 57::559
    [Crossref] [Google Scholar]
  100. 100.
    Szczuka A, Korczyńska J, Wnuk A, Symonowicz B, Szwacka AG, et al. 2013.. The effects of serotonin, dopamine, octopamine and tyramine on behavior of workers of the ant Formica polyctena during dyadic aggression tests. . Acta Neurobiol. Exp. 73::495520
    [Crossref] [Google Scholar]
  101. 101.
    Tarry D. 1969.. Dicrocoelium dendriticum: the life cycle in Britain. . J. Helminthol. 43::40316
    [Crossref] [Google Scholar]
  102. 102.
    Taylor TN, Remy W, Hass H. 1992.. Parasitism in a 400-million-year-old green alga. . Nature 357::49394
    [Crossref] [Google Scholar]
  103. 103.
    Thomas F, Schmidt-Rhaesa A, Martin G, Manu C, Durand P, Renaud F. 2002.. Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts?. J. Evol. Biol. 15::35661
    [Crossref] [Google Scholar]
  104. 104.
    Trinh T, Ouellette R, de Bekker C. 2021.. Getting lost: the fungal hijacking of ant foraging behaviour in space and time. . Anim. Behav. 181::16584
    [Crossref] [Google Scholar]
  105. 105.
    Valdes JJ, Cameron JE, Cole RJ. 1985.. Aflatrem: a tremorgenic mycotoxin with acute neurotoxic effects. . Environ. Health Perspect. 62::45963
    [Crossref] [Google Scholar]
  106. 106.
    van Houte S, Ros VI, Mastenbroek TG, Vendrig NJ, Hoover K, et al. 2012.. Protein tyrosine phosphatase-induced hyperactivity is a conserved strategy of a subset of baculoviruses to manipulate lepidopteran host behavior. . PLOS ONE 7:(10):e46933
    [Crossref] [Google Scholar]
  107. 107.
    van Houte S, Ros VI, van Oers MM. 2013.. Walking with insects: molecular mechanisms behind parasitic manipulation of host behaviour. . Mol. Ecol. 22::345875
    [Crossref] [Google Scholar]
  108. 108.
    Wang W, Barnaby JY, Tada Y, Li H, Tör M, et al. 2011.. Timing of plant immune responses by a central circadian regulator. . Nature 470::11014
    [Crossref] [Google Scholar]
  109. 109.
    Westwood ML, O'Donnell AJ, de Bekker C, Lively CM, Zuk M, Reece SE. 2019.. The evolutionary ecology of circadian rhythms in infection. . Nat. Ecol. Evol. 3::55260
    [Crossref] [Google Scholar]
  110. 110.
    Wilding N. 1970.. Entomophthora conidia in the air-spora. . Microbiology 62::14957
    [Google Scholar]
  111. 111.
    Will I, Attardo GM, de Bekker C. 2023.. Multiomic interpretation of fungus-infected ant metabolomes during manipulated summit disease. . Sci. Rep. 13::14363
    [Crossref] [Google Scholar]
  112. 112.
    Will I, Beckerson WC, de Bekker C. 2023.. Using machine learning to predict protein–protein interactions between a zombie ant fungus and its carpenter ant host. . Sci. Rep. 13::13821
    [Crossref] [Google Scholar]
  113. 113.
    Will I, Das B, Trinh T, Brachmann A, Ohm RA, de Bekker C. 2020.. Genetic underpinnings of host manipulation by Ophiocordyceps as revealed by comparative transcriptomics. . G3 10::227596
    [Crossref] [Google Scholar]
  114. 114.
    Will I, Linehan S, Jenkins DG, de Bekker C. 2023.. Natural history and ecological effects on the establishment and fate of Florida carpenter ant cadavers infected by the parasitic manipulator Ophiocordyceps camponoti-floridani. . Funct. Ecol. 37::88699
    [Crossref] [Google Scholar]
  115. 115.
    Wilson BJ, Wilson CH. 1964.. Toxin from Aspergillus flavus: production on food materials of a substance causing tremors in mice. . Science 144::17778
    [Crossref] [Google Scholar]
  116. 116.
    Xu ZH, Tran NL, Wang Y, Zhang GD, Dao VM, et al. 2022.. Phylogeny and morphology of Ophiocordyceps puluongensis sp. nov. (Ophiocordycipitaceae, Hypocreales), a new fungal pathogen on termites from Vietnam. . J. Invert. Pathol. 192::107771
    [Crossref] [Google Scholar]
  117. 117.
    Yang Z, Yu Y, Zhang V, Tian Y, Qi W, Wang L. 2015.. Octopamine mediates starvation-induced hyperactivity in adult Drosophila. . PNAS 112::521924
    [Crossref] [Google Scholar]
  118. 118.
    Zhang S, An S, Hoover K, Li Z, Li X, et al. 2018.. Host miRNAs are involved in hormonal regulation of HaSNPV-triggered climbing behaviour in Helicoverpa armigera. . Mol. Ecol. 27::45975
    [Crossref] [Google Scholar]
  119. 119.
    Zhang X, Harding BW, Aggad D, Courtine D, Chen JX, et al. 2021.. Antagonistic fungal enterotoxins intersect at multiple levels with host innate immune defences. . PLOS Genet. 17::e1009600
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-micro-041522-092522
Loading
/content/journals/10.1146/annurev-micro-041522-092522
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error