Fungi That Infect Insects: Altering Host Behavior and Beyond

1. Vega FE, Meyling NV, Luangsa-Ard JJ, Blackwell M (2012) Fungal entomopathogens. In: Vega F, Kaya HK, editors. Insect Pathology, 2nd ed. San Diego: Academic Press; pp. 171–220.

2. de Faria MR, Wraight SP (2007) Mycoinsecticides and Mycoacaricides: A comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43: 237–256.

3. Hu X, Xiao G, Zheng P, Shang Y, Su Y, et al. (2014) Trajectory and genomic determinants of fungal-pathogen speciation and host adaptation. Proc Natl Acad Sci U S A 111: 16796–16801. doi: 10.1073/pnas.1412662111 25368161

4. Sung GH, Hywel-Jones NL, Sung JM, Luangsa-Ard JJ, Shrestha B, et al. (2007) Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Stud Mycol 57: 5–59. doi: 10.3114/sim.2007.57.01 18490993

5. Gao Q, Jin K, Ying SH, Zhang Y, Xiao G, et al. (2011) Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genet 7: e1001264. doi: 10.1371/journal.pgen.1001264 21253567

6. Zheng P, Xia Y, Xiao G, Xiong C, Hu X, et al. (2011) Genome sequence of the insect pathogenic fungus Cordyceps militaris, a valued traditional Chinese medicine. Genome Biol 12: R116. doi: 10.1186/gb-2011-12-11-r116 22112802

7. Bushley KE, Raja R, Jaiswal P, Cumbie JS, Nonogaki M, et al. (2013) The genome of Tolypocladium inflatum: evolution, organization, and expression of the cyclosporin biosynthetic gene cluster. PLoS Genet 9: e1003496. doi: 10.1371/journal.pgen.1003496 23818858

8. Hu X, Zhang YJ, Xiao G, Zheng P, Xia Y, et al. (2013) Genome survey uncovers the secrets of sex and lifestyle in caterpillar fungus. Chinese Sci Bull 58: 2846–2854.

9. Andersen SB, Gerritsma S, Yusah KM, Mayntz D, Hywel-Jones NL, et al. (2009) The life of a dead ant: the expression of an adaptive extended phenotype. Am Nat 174: 424–433. doi: 10.1086/603640 19627240

10. Heinze J, Walter B (2010) Moribund ants leave their nests to die in social isolation. Curr Biol 20: 249–252. doi: 10.1016/j.cub.2009.12.031 20116243

11. Yanagawa A, Fujiwara-Tsujii N, Akino T, Yoshimura T, Yanagawa T, et al. (2011) Musty odor of entomopathogens enhances disease-prevention behaviors in the termite Coptotermes formosanus. J Invertebr Pathol 108: 1–6. doi: 10.1016/j.jip.2011.06.001 21683707

12. Behie SW, Zelisko PM, Bidochka MJ (2012) Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science 336: 1576–1577. doi: 10.1126/science.1222289 22723421

13. de Bekker C, Quevillon LE, Smith PB, Fleming KR, Ghosh D, et al. (2014) Species-specific ant brain manipulation by a specialized fungal parasite. BMC Evol Biol 14: 166. doi: 10.1186/s12862-014-0166-3 25085339

14. 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. doi: 10.1371/journal.pone.0017024 21399679

15. 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: 44–52. doi: 10.1016/j.funbio.2014.10.008 25601148

16. Libersat F, Delago A, Gal R (2009) Manipulation of host behavior by parasitic insects and insect parasites. Annu Rev Entomol 54: 189–207. doi: 10.1146/annurev.ento.54.110807.090556 19067631

17. Hughes DP, Andersen SB, Hywel-Jones NL, Himaman W, Billen J, et al. (2011) Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. BMC Ecol 11: 13. doi: 10.1186/1472-6785-11-13 21554670

18. Roy HE, Steinkraus DC, Eilenberg J, Hajek AE, Pell JK (2006) Bizarre interactions and endgames: entomopathogenic fungi and their arthropod hosts. Annu Rev Entomol 51: 331–357. 16332215

19. Cremer S, Armitage SA, Schmid-Hempel P (2007) Social immunity. Curr Biol 17: R693–R702. 17714663

20. Wilson-Rich N, Spivak M, Fefferman NH, Starks PT (2009) Genetic, individual, and group facilitation of disease resistance in insect societies. Annu Rev Entomol 54: 405–423. doi: 10.1146/annurev.ento.53.103106.093301 18793100

21. Simola DF, Wissler L, Donahue G, Waterhouse RM, Helmkampf M, et al. (2013) Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality. Genome Res 23: 1235–1247. doi: 10.1101/gr.155408.113 23636946

22. Yanagawa A, Shimizu S (2007) Resistance of the termite, Coptotermes formosanus Shiraki to Metarhizium anisopliae due to grooming. BioControl 52: 75–85.

23. Ugelvig LV, Cremer S (2007) Social prophylaxis: group interaction promotes collective immunity in ant colonies. Curr Biol 17: 1967–1971. 17980590

24. Tragust S, Mitteregger B, Barone V, Konrad M, Ugelvig LV, et al. (2013) Ants disinfect fungus-exposed brood by oral uptake and spread of their poison. Curr Biol 23: 76–82. doi: 10.1016/j.cub.2012.11.034 23246409

25. Bulmer MS, Bachelet I, Raman R, Rosengaus RB, Sasisekharan R (2009) Targeting an antimicrobial effector function in insect immunity as a pest control strategy. Proc Natl Acad Sci U S A 106: 12652–12657. doi: 10.1073/pnas.0904063106 19506247

26. Blanford S, Thomas M B (1999) Host thermal biology: the key to understanding host–pathogen interactions and microbial pest control? Agric For Entomol 1: 195–202.

27. Wang Y, Yang P, Cui F, Kang L (2013) Altered immunity in crowded locust reduced fungal (Metarhizium anisopliae) pathogenesis. PLoS Pathog 9: e1003102. doi: 10.1371/journal.ppat.1003102 23326229

28. van Houte S, Ros VI, van Oers MM (2013) Walking with insects: molecular mechanisms behind parasitic manipulation of host behaviour. Mol Ecol 22: 3458–3475. doi: 10.1111/mec.12307 23742168

29. Hoover K, Grove M, Gardner M, Hughes DP, McNeil J, et al. (2011) A gene for an extended phenotype. Science 333: 1401. doi: 10.1126/science.1209199 21903803

30. Katsuma S, Koyano Y, Kang W, Kokusho R, Kamita SG, et al. (2012) The baculovirus uses a captured host phosphatase to induce enhanced locomotory activity in host caterpillars. PLoS Pathog 8: e1002644. doi: 10.1371/journal.ppat.1002644 22496662

31. Pedras MS, Irina Zaharia L, Ward DE. (2002) The destruxins: synthesis, biosynthesis, biotransformation, and biological activity. Phytochemistry 59: 579–596. 11867090

32. Wang B, Kang Q, Lu Y, Bai L, Wang C (2012) Unveiling the biosynthetic puzzle of destruxins in Metarhizium species. Proc Natl Acad Sci U S A 109: 1287–1292. doi: 10.1073/pnas.1115983109 22232661

33. Perry CJ, Barron AB (2013) Neural mechanisms of reward in insects. Annu Rev Entomol 58: 543–562. doi: 10.1146/annurev-ento-120811-153631 23020615

34. Wang X, Kang L (2014) Molecular mechanisms of phase change in locusts. Annu Rev Entomol 59: 225–244. doi: 10.1146/annurev-ento-011613-162019 24160426

35. Wada-Katsumata A, Yamaoka R, Aonuma H (2011) Social interactions influence dopamine and octopamine homeostasis in the brain of the ant Formica japonica. J Exp Biol 214: 1707–1713. doi: 10.1242/jeb.051565 21525317

36. Szczuka A, Korczyńska J, Wnuk A, Symonowicz B, Szwacka GA, 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: 495–520.