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Pathogenic fungus uses volatiles to entice male flies into fatal matings with infected female cadavers

  • Ryan MJ, Rand AS. Species recognition and sexual selection as a unitary problem in animal communication. Evolution. 1993;47:647–57.

    PubMed 
    Article 

    Google Scholar 

  • Trivers RL. Parental Investment and Sexual Selection. In: Campbell BG, (ed). Sexual Selection and the Descent of Man. Aldine Publishing Company; 1972. p. 136–79.

    Google Scholar 

  • Andersson M. Sexual selection. Sexual Selection. Princeton: Princeton University Press; 1994.

    Chapter 

    Google Scholar 

  • Schiestl FP, Ayasse M, Paulus HF, Löfstedt C, Hansson BS, Ibarra F, et al. Sex pheromone mimicry in the early spider orchid (Ophrys sphegodes): Patters of hydrocarbons as the key mechanism for pollination by sexual deception. J Comp Physiol – A Sens, Neural, Behav Physiol. 2000;186:567–74.

    CAS 
    Article 

    Google Scholar 

  • Cohen C, Liltved WR, Colville JF, Bytebier B, Johnson SD. Sexual deception of a beetle pollinator through floral mimicry. Curr Biol. 2021;31:1962–1969. e6.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Hayashi T, Bohman B, Scaffidi A, Peakall R, Flematti GR. An unusual tricosatriene is crucial for male fungus gnat attraction and exploitation by sexually deceptive Pterostylis orchids. Curr Biol. 2021;31:1954–1961. e7.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Hansen AN, De Fine Licht HH. Logistic growth of the host-specific obligate insect pathogenic fungus Entomophthora muscae in house flies (Musca domestica). J Appl Entomol. 2017;141:583–6.

    CAS 
    Article 

    Google Scholar 

  • Schmid-Hempel P Evolutionary parasitology. 2011. Oxford University Press.

  • Helluy S, Thomas F. Effects of Microphallus papillorobustus (Platyhelminthes: Trematoda) on serotonergic immunoreactivity and neuronal architecture in the brain of Gammarus insensibilis (Crustacea: Amphipoda). Proc R Soc B: Biol Sci. 2003;270:563–8.

    CAS 
    Article 

    Google Scholar 

  • Hoover K, Grove M, Gardner M. A gene for an extended phenotype. Science. 2011;333:1401. others.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Adamo SA. Parasites: evolution’s neurobiologists. J Exp Biol. 2013;216:3–10.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • de Bekker C, Ohm RA, Loreto RG. Gene expression during zombie ant biting behavior reflects the complexity underlying fungal parasitic behavioral manipulation. BMC Genomics. 2015;16:620. others.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Ros VID, Van Houte S, Hemerik L, Van Oers MM. Baculovirus-induced tree-top disease: How extended is the role of egt as a gene for the extended phenotype? Mol Ecol. 2015;24:249–58.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Botnevik CF, Malagocka J, Jensen AB, Fredensborg BL. Relative effects of temperature, light, and humidity on clinging behavior of metacercariae-infected ants. J Parasitol. 2016;102:495–500.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Małagocka J, Jensen AB, Eilenberg J. Pandora formicae, a specialist ant pathogenic fungus: New insights into biology and taxonomy. J Invertebr Pathol. 2017;143:108–14.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Hughes DP, Libersat F. Neuroparasitology of parasite-insect associations. Annu Rev Entomol. 2018;63:471–87.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Hojo MK, Pierce NE, Tsuji K. Lycaenid caterpillar secretions manipulate attendant ant behavior. Curr Biol. 2015;25:2260–4.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Gal R, Libersat F. A wasp manipulates neuronal activity in the sub-esophageal ganglion to decrease the drive for walking in its cockroach prey. PLoS ONE. 2010;5:e10019.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Keesey IW, Koerte S, Khallaf MA, Retzke T, Guillou A, Grosse-Wilde E, et al. Pathogenic bacteria enhance dispersal through alteration of Drosophila social communication. Nat Commun. 2017;8:265.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Zhang X, Machado RAR, Van Doan C, Arce CCM, Hu L, Robert CAM. Entomopathogenic nematodes increase predation success by inducing cadaver volatiles that attract healthy herbivores. eLife. 2019;8:e46668.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • George J, Jenkins NE, Blanford S, Thomas MB, Baker TC. Malaria mosquitoes attracted by fatal fungus. PLoS ONE. 2013;8:e62632.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Trandem N, Bhattarai UR, Westrum K, Knudsen GK, Klingen I. Fatal attraction: male spider mites prefer females killed by the mite-pathogenic fungus Neozygites floridana. J Invertebr Pathol. 2015;128:6–13.

    PubMed 
    Article 

    Google Scholar 

  • Evans WS, Wong A, Hardy M, Currie RW, Vanderwel D. Evidence that the factor used by the tapeworm, Hymenolepis diminuta, to direct the foraging of its intermediate host, Tribolium confusum, is a volatile attractant. J Parasitol. 1998;84:1098–101.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Shostak AW, Smyth KA. Activity of flour beetles (Tribolium confusum) in the presence of feces from rats infected with rat tapeworm (Hymenolepis diminuta). Can J Zool. 1998;76:1472–9.

    Article 

    Google Scholar 

  • Shea JF. Lack of preference for infective faeces in Hymenolepis diminuta-infected beetles (Tenebrio molitor). J Helminthol. 2007;81:293–9.

    PubMed 
    Article 

    Google Scholar 

  • Mauck KE, De Moraes CM, Mescher MC. Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts. Proc Natl Acad Sci USA. 2010;107:3600–5.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Dawkins R. The extended phenotype. Oxford: Oxdord University Press; 1982.

    Google Scholar 

  • Van Houte S, Ros VID, Van Oers MM. Walking with insects: Molecular mechanisms behind parasitic manipulation of host behaviour. Mol Ecol. 2013;22:3458–75.

    PubMed 
    Article 

    Google Scholar 

  • de Bekker C, Beckerson WC, Elya C. Mechanisms behind the madness: how do zombie-making fungal entomopathogens affect host behavior to increase transmission? mBio. 2021;12:e01872–21.

    PubMed Central 
    Article 

    Google Scholar 

  • Lefévre T, Lebarbenchon C, Gauthier-Clerc M, Missé D, Poulin R, Thomas F, et al. The ecological significance of manipulative parasites. Trends Ecol Evolution. 2009;24:41–48.

    Article 

    Google Scholar 

  • Kalsbeek V, Pell JK, Steenberg T. Sporulation by Entomophthora schizophorae (Zygomycetes: Entomophthorales) from housefly cadavers and the persistence of primary conidia at constant temperatures and relative humidities. J Invertebr Pathol. 2001;77:149–57.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • de Ruiter J, Arnbjerg-Nielsen SF, Herren P, Høier F, De Fine Licht HH, Jensen KH. Fungal artillery of zombie flies: infectious spore dispersal using a soft water cannon. J R Soc Interface. 2019;16:20190448.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Lovett B, Macias A, Stajich JE, Cooley J, Eilenberg J, de Fine Licht HH, et al. Behavioral betrayal: how select fungal parasites enlist living insects to do their bidding. PLoS Pathog. 2020;16:e1008598.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Moller AP. A fungus infecting domestic flies manipulates sexual behaviour of its host. Behav Ecol Sociobiol. 1993;33:403–7.

    Google Scholar 

  • Murvosh CM, Fye RL, LaBrecque GC. Studies on the mating behavior of the house fly, Musca Domestica L. Ohio J Sci. 1964;64:264–71.

    Google Scholar 

  • Tobin EN, Stoffolano JG. The courtship of Musca species found in North America. II. The face fly, Musca autumnalis, and a comparison. Ann Entomological Soc Am. 1973;66:1329–34.

    Article 

    Google Scholar 

  • Goulson D, Bristow L, Elderfield E, Brinklow K, Parry-Jones B, Chapman JW. Size, Symmetry, and sexual selection in the housefly, Musca domestica. Evolution. 1999;53:527–34.

    PubMed 
    Article 

    Google Scholar 

  • Zurek L, Wes Watson D, Krasnoff SB, Schal C. Effect of the entomopathogenic fungus, Entomophthora muscae (Zygomycetes: Entomophthoraceae), on sex pheromone and other cuticular hydrocarbons of the house fly, Musca domestica. J Invertebr Pathol. 2002;80:171–6.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Rogoff WM, Beltz AD, Johnsen JO, Plapp FW. A sex pheromone in the housefly, Musca domestica L. J Insect Physiol. 1964;10:239–46.

    CAS 
    Article 

    Google Scholar 

  • Adams TS, Holt GG. Effect of pheromone components when applied to different models on male sexual behaviour in the housefly, Musca domestica. J Insect Physiol. 1987;33:9–18.

    CAS 
    Article 

    Google Scholar 

  • Carlson DA, Mayer MS, Silhacek DL, James JD, Beroza M, Bierl BA, et al. Sex attractant pheromone of the house fly: Isolation, identification and synthesis. Science. 1971;174:76–78.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Adams TS, Nelson DR, Fatland CL. Effect of methylalkanes on male house fly, Musca domestica, sexual behavior. J Insect Physiol. 1995;41:443–9.

    CAS 
    Article 

    Google Scholar 

  • Noorman N, Otter CJ. The effects of laboratory culturing on (Z)-9-tricosene (muscalure) quantities on female houseflies. Entomologia Experimentalis et Applicata. 2001;101:69–80.

    CAS 
    Article 

    Google Scholar 

  • Uebel EC, Schwarz M, Lusby WR, Miller RW, Sonnet PE. Cuticular nonhydrocarbons of the female house fly and their evaluation as mating stimulants. Lloydia. 1978;41:63–67.

    CAS 

    Google Scholar 

  • Blomquist GJ, Ginzel MD. Chemical ecology, biochemistry, and molecular biology of insect hydrocarbons. Annu Rev Entomol. 2021;66:45–60.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Lebreton S, Borrero-Echeverry F, Gonzalez F, Solum M, Wallin EA, Hedenström E, et al. A Drosophila female pheromone elicits species-specific long-range attraction via an olfactory channel with dual specificity for sex and food. BMC Biol. 2017;15:88.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Krasnoff SB, Watson DW, Gibson DM, Kwan EC. 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. 1995;41:895–903.

    CAS 
    Article 

    Google Scholar 

  • Friard O, Gamba M. BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol Evolution. 2016;7:1325–30.

    Article 

    Google Scholar 

  • Quan AS, Eisen MB. The ecology of the Drosophila-yeast mutualism in wineries. PLOS ONE. 2018;13:e0196440.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • van Den Dool H, Dec, Kratz P. A generalization of the retention index system including linear temperature programmed gas-liquid partition chromatography. J Chromatogr A. 1963;11:463–71.

    Article 

    Google Scholar 

  • Nelson DR, Dillwith JW, Blomquist GJ. Cuticular hydrocarbons of the house fly, Musca domestica. Insect Biochem. 1981;11:187–97.

    CAS 
    Article 

    Google Scholar 

  • Bagnères AG, Morgan ED. A simple method for analysis of insect cuticular hydrocarbons. J Chem Ecol. 1990;16:3263–76.

    PubMed 
    Article 

    Google Scholar 

  • Stránský K, Jursík T, Vítek A, Skořepa J. An improved method of characterizing fatty acids by equivalent chain length values. J High Resolut Chromatogr. 1992;15:730–40.

    Article 

    Google Scholar 

  • Stránský K, Zarevúcka M, Valterová I, Wimmer Z. Gas chromatographic retention data of wax esters. J Chromatogr A. 2006;1128:208–19.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Carlson DA, Bernier UR, Sutton BD. Elution patterns from capillary GC for methyl-branched alkanes. J Chem Ecol. 1998;24:1845–65.

    CAS 
    Article 

    Google Scholar 

  • Mpuru S, Blomquist GJ, Schal C, Roux M, Kuenzli M, Dusticier G, et al. Effect of age and sex on the production of internal and external hydrocarbons and pheromones in the housefly, Musca domestica. Insect Biochem Mol Biol. 2001;31:139–55.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Gulias Gomes CC, Trigo JR, Eiras ÁE. Sex pheromone of the American warble fly, Dermatobia hominis: The role of cuticular hydrocarbons. J Chem Ecol. 2008;34:636–46.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Zhang LX, Yun YF, Liang YZ, Cao DS. Discovery of mass spectral characteristics and automatic identification of wax esters from gas chromatography mass spectrometry data. J Chromatogr A. 2010;1217:3695–701.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Bray NL, Pimentel H, Melsted P, Pachter L. Near-optimal probabilistic RNA-seq quantification. Nat Biotechnol. 2016;34:525–7.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015;67:1–48.

    Article 
    CAS 

    Google Scholar 

  • Becher PG, Verschut V, Bibb MJ, Bush MJ, Molnár BP, Barane E, et al. Developmentally regulated volatiles geosmin and 2-methylisoborneol attract a soil arthropod to Streptomyces bacteria promoting spore dispersal. Nat Microbiol. 2020;5:821–9.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Lê S, Josse J, Husson F. FactoMineR: An R package for multivariate analysis. J Stat Softw. 2008;25:1–18.

    Article 

    Google Scholar 

  • Darbro JM, Millar JG, McElfresh JS, Mullens BA. Survey of muscalure [(Z)-9-tricosene] on house flies (Diptera: Muscidae) from field populations in California. Environ Entomol. 2005;34:1418–25.

    CAS 
    Article 

    Google Scholar 

  • Butler SM, Moon RD, Hinkle NC, Millar JG, Mcelfresh JS, Mullens BA. Characterization of age and cuticular hydrocarbon variation in mating pairs of house fly, Musca domestica, collected in the field. Med Vet Entomol. 2009;23:426–42.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Eder M, Sanchez I, Brice C, Camarasa C, Legras JL, Dequin S. QTL mapping of volatile compound production in Saccharomyces cerevisiae during alcoholic fermentation. BMC Genomics. 2018;19:166.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Vranová E, Coman D, Gruissem W. Network analysis of the MVA and MEP pathways for isoprenoid synthesis. Annu Rev Plant Biol. 2013;64:665–700.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Saerens SMG, Verstrepen KJ, Van Laere SDM, Voet ARD, Van Dijck P, Delvaux FR, et al. The Saccharomyces cerevisiae EHT1 and EEB1 genes encode novel enzymes with medium-chain fatty acid ethyl ester synthesis and hydrolysis capacity. J Biol Chem. 2006;281:4446–56.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Saerens SMG, Delvaux F, Verstrepen KJ, Van Dijck P, Thevelein JM, Delvaux FR. Parameters affecting ethyl ester production by Saccharomyces cerevisiae during fermentation. Appl Environ Microbiol. 2008;74:454–61.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Cooley JR, Marshall DC, Hill KBR. A specialized fungal parasite (Massospora cicadina) hijacks the sexual signals of periodical cicadas (Hemiptera: Cicadidae: Magicicada). Sci Rep. 2018;8:1432.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Zhang X-M. Floral volatile sesquiterpenes of Elsholtzia rugulosa (Lamiaceae) selectively attract Asian honey bees. J Appl Entomol. 2018;142:359–62.

    CAS 
    Article 

    Google Scholar 

  • Haber AI, Sims JW, Mescher MC, De Moraes CM, Carr DE. A key floral scent component (β-trans-bergamotene) drives pollinator preferences independently of pollen rewards in seep monkeyflower. Funct Ecol. 2019;33:218–28.

    Article 

    Google Scholar 

  • Mithöfer A, Boland W. Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol. 2012;63:431–50.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Stanjek V, Herhaus C, Ritgen U, Boland W, Städler E. Changes in the leaf surface chemistry of Apium graveolens (apiaceae) stimulated by jasmonic acid and perceived by a specialist insect. Helvetica Chim Acta. 1997;80:1408–20.

    CAS 
    Article 

    Google Scholar 

  • Ding Y, Huffaker A, Köllner TG, Weckwerth P, Robert CAM, Spencer JL, et al. Selinene volatiles are essential precursors for maize defense promoting fungal pathogen resistance. Plant Physiol. 2017;175:1455–68.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Könen PP, Wüst M. Analysis of sesquiterpene hydrocarbons in grape berry exocarp (Vitis vinifera L.) using in vivo-labeling and comprehensive two-dimensional gas chromatography–mass spectrometry (GC×GC–MS). Beilstein J Org Chem. 2019;15:1945–61.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Lam K, Tsang M, Labrie A, Gries R, Gries G. Semiochemical-mediated oviposition avoidance by female house flies, Musca domestica, on animal feces colonized with harmful fungi. J Chem Ecol. 2010;36:141–7.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Phillips RD, Bohman B, Peakall R. Pollination by nectar‐foraging pompilid wasps: a new specialized pollination strategy for the Australian flora. Plant Biology 2021;23:702–10.

  • Spieth HT. Courtship behavior in Drosophila. Annu Rev Entomol. 1974;19:385–405.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Grosjean Y, Rytz R, Farine JP, Abuin L, Cortot J, Jefferis GSXE, et al. An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature. 2011;478:236–40.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Mullens BA, Rodrigues JL, Meyer JA. An epizootiological study of Entomophthora muscae in muscoid fly populations on southern california poultry facilities, with emphasis on Musca domestica. Hilgardia. 1987;55:1–41.

    Article 

    Google Scholar 

  • Watson DW, Petersen JJ. Sexual activity of male Musca domestica (Diptera: Muscidae) infected with Entomophthora muscae (Entomophthoraceae: Entomophthorales). Biol Control. 1993;3:22–26.

    Article 

    Google Scholar 

  • van Huis A, Oonincx DGAB, Rojo S, Tomberlin JK. Insects as feed: house fly or black soldier fly? J Insects Food Feed. 2020;6:221–9.

    Article 

    Google Scholar 

  • Khamesipour F, Lankarani KB, Honarvar B, Kwenti TE. A systematic review of human pathogens carried by the housefly (Musca domestica L.). BMC Public Health. 2018;18:1049.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Biedermann PHW, De Fine Licht HH, Rohlfs M. Evolutionary chemo-ecology of insect-fungus interactions: still in its infancy but advancing. Fungal Ecol. 2019;38:1–6.

    Article 

    Google Scholar 


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