Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-745bb68f8f-l4dxg Total loading time: 0 Render date: 2025-01-25T17:43:28.397Z Has data issue: false hasContentIssue false

Chapter Six - The microbiome and host behaviour

Published online by Cambridge University Press:  07 March 2020

By
Anne Lizé  and
Zenobia Lewis
Edited by
Rachael E. Antwis ,
Xavier A. Harrison  and
Michael J. Cox
Rachael E. Antwis
Affiliation:
University of Salford
Xavier A. Harrison
Affiliation:
University of Exeter
Michael J. Cox
Affiliation:
University of Birmingham
Get access

Summary

The potential for microorganisms to affect host behaviour has been recognised for decades, particularly with respect to parasites, but research into the wider influence of microorganisms on host behaviour and communication is now also gaining more interest. Microbial communities and associated metabolites can affect satiation, cravings and dysphoria that can influence feeding behaviour and nutrient acquisition. Microbial communities can also synthesise hormones that are analogous in structure and function to those produced by the host, as well as degrade or metabolise host-derived hormones. This can affect host mood and stress, as well as reproductive behaviours and fecundity. The gut microbiome also plays a key role in normal cognitive development of mammals, including aspects such as learning and memory. Furthermore, microbial metabolites are critical for scent communication, such as pheromone production, across many different species, and may also play a role in pollinator attraction by plants. However, the literature is largely biased towards mammals, and in many cases the mechanisms underlying microorganism-induced host behavioural changes still need identifying.

Keywords

cognitioncommunicationforaginghormoneslearningmemorymovementreproductionsocial interactionsstress
Type
Chapter
Information
Microbiomes of Soils, Plants and Animals
An Integrated Approach
 , pp. 98 - 121
Publisher: Cambridge University Press
Print publication year: 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abbott, J. (2014) Self-medication in insects: Current evidence and future perspectives. Ecological Entomology, 39, 273–280.Google Scholar
Abildgaard, A, Elfving, B, Hokland, M, et al. (2017) Probiotic treatment reduces depressive-like behaviour in rats independently of diet. Psychoneuroendocrinology, 79, 40–48.CrossRefGoogle ScholarPubMed
Albone, ES. (1984) Mammalian Semiochemistry. London: John Wiley.Google Scholar
Alcock, J, Maley, CC, Aktipis, CA. (2014) Is eating behaviour manipulated by the gastrointestinal microbiota? Evolutionary pressures and potential mechanisms. BioEssays, 36, 940–949.CrossRefGoogle ScholarPubMed
Alvarez-Pérez, S, Herrera, CM, de Vega, C. (2012) Zooming in on floral nectar: A first exploration of nectar-associated bacteria in wild plant communities. FEMS Microbiology Ecology, 80, 591–602.Google Scholar
Andersen, SB, Ferrari, M, Evans, HC, et al. (2012) Disease dynamics in a specialized parasite of ant societies. PLoS ONE, 7, e36352.CrossRefGoogle Scholar
Antwis, RE, Lea, JMD, Unwin, B, et al. (2018) Gut microbiome composition is associated with spatial structuring and social interactions in semi-feral Welsh mountain ponies. Microbiome, 6, 207.Google Scholar
Antwis, RE, Edwards, KL, Unwin, B, et al. (2019) Rare gut microbiota associated with breeding success, hormone metabolites and ovarian cycle phase in the critically endangered eastern black rhino. Microbiome, 7, 27.Google Scholar
Araújo, J, Hughes, DP. (2016) Diversity of entomopathogenic fungi: Which groups conquered the insect body? Advances in Genetics, 94, 1–39.CrossRefGoogle ScholarPubMed
Archie, EA, Theis, KR. (2011) Animal behaviour meets microbial ecology. Animal Behaviour, 82, 425–436.CrossRefGoogle Scholar
Archie, EA, Tung, J. (2015) Social behavior and the microbiome. Current Opinion in Behavioral Sciences, 6, 28–34.Google Scholar
Arentsen, T, Raith, H, Qian, Y, et al. (2015) Host microbiota modulates development of social preference in mice. Microbial Ecology in Health and Disease, 26, 29719.CrossRefGoogle ScholarPubMed
Arseneault-Bréard, J, Rondeau, I, Gilbert, K, et al. (2012) Combination of Lactobacillus helveticus R0052 and Bifidobacterium longum R0175 reduces post-myocardial infarction depression symptoms and restores intestinal permeability in a rat model. The British Journal of Nutrition, 107, 1793–1799.CrossRefGoogle ScholarPubMed
Babikova, Z, Gilbert, L, Bruce, TJA, et al. (2013) Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecology Letters, 16, 835–843.CrossRefGoogle ScholarPubMed
Bailey, MT, Dowd, SE, Parry, NM, et al. (2010) Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium. Infection and Immunity, 78, 1509–1519.CrossRefGoogle ScholarPubMed
Baker, JM, Al-Nakkash, L, Herbst-Kralovetz, MM. (2017) Estrogen–gut microbiome axis: Physiological and clinical implications. Maturitas, 103, 45–53.Google Scholar
Baldwin, IT, Schultz, JC. (1983) Rapid changes in tree leaf chemistry induced by damage – Evidence for communication between plants. Science, 221, 277–279.CrossRefGoogle ScholarPubMed
Berdoy, M, Webster, JP, Macdonald, DW. (2000) Fatal attraction in Toxoplasma-infected rats: A case of parasite manipulation of its mammalian host. Proceedings of the Royal Society B: Biological Sciences, 267, 1591–1594.Google Scholar
Biedrzycki, ML, Bais, HP. (2010) Kin recognition in plants: A mysterious behaviour unsolved. The Journal of Experimental Botany, 61, 4123–4128.CrossRefGoogle ScholarPubMed
Biedrzycki, ML, Jilany, TA, Dudley, SA, et al. (2010) Root exudates mediate kin recognition in plants. Communicative & Integrative Biology, 3, 28–35.Google Scholar
Bloss, J, Acree, TE, Bloss, JM, et al. (2002) Potential use of chemical cues for colony-mate recognition in the big brown bat, Eptesicus fuscus. Journal of Chemical Ecology, 28, 819–834.Google Scholar
Blunk, H. (1922) Die lebensgeschichte der im gelbrand schmarotzenden saitenwürmer. Zoologische Anzeiger, 54, 110–132.Google Scholar
Bonaz, B, Bazin, T, Pellissier, S. (2018) The vagus nerve at the interface of the microbiota–gut–brain axis. Frontiers in Neurosciences, 12, 49.Google Scholar
Bravo, JA, Forsythe, P, Chew, MV, et al. (2011) Ingestion of Lactobacillus strain regulates emotional behaviour and central GABA receptor expression in a mouse via the vagus nerve. Proceedings of the National Academy of Sciences, 108, 16050–16055.Google Scholar
Brucker, RM, Bordenstein, SR. (2013) The hologenomic basis of speciation: Gut bacteria cause hybrid lethality in the genus Nasonia. Science, 341, 667–669.CrossRefGoogle ScholarPubMed
Brummel, T, Ching, A, Seroude, L, et al. (2004) Drosophila lifespan enhancement by exogenous bacteria. Proceedings of the National Academy of Sciences, 101, 12974–12979.Google Scholar
Caldwell, KN, Anderson, GL, Williams, PL, et al. (2003) Attraction of a free-living nematode, Caenorhabditis elegans, to foodborne pathogenic bacteria and its potential as a vector of Salmonella poona for preharvest contamination of cantaloupe. Journal of Food Protection, 66, 1964–1971.Google Scholar
Carlson, AL, Xia, K, Azcarate-Peril, MA, et al. (2018) Infant gut microbiome associated with cognitive development. Biological Psychiatry, 83, 148–159.Google Scholar
Carnevali, O, Avella, MA, Gioacchini, G (2013) Effects of probiotic administration on zebra fish development and reproduction. General and Comparative Endocrinology, 188, 297–302.Google Scholar
Cézilly, F, Grégoire, A, Bertin, A. (2000) Conflict between cooccurring manipulative parasites? An experimental study of the joint influence of two acanthocephalan parasites on the behaviour of Gammarus pulex. Parasitology, 120, 625–630.CrossRefGoogle ScholarPubMed
Charlat, S, Reuter, M, Dyson, EA, et al. (2007) Male-killing bacteria trigger a cycle of increasing male fatigue and female promiscuity. Current Biology, 17, 273–277.Google Scholar
Clemente, JC, Ursell, LK, Parfrey, LW, et al. (2012) The impact of the gut microbiota on human health: An integrative view. Cell, 148, 1258–1270.Google Scholar
Cryan, JF, Dinan, TG. (2012) Mind-altering microorganisms: The impact of the gut microbiota on brain and behaviour. Nature Reviews Neuroscience, 13, 701–712.Google Scholar
Davis, DJ, Bryda, EC, Gillepsie, CH, et al. (2016) Microbial modulation of behavior and stress responses in zebrafish larvae. Behavioural Brain Research, 311, 219–227.Google Scholar
de Crespigny, FEC, Pitt, TD, Wedell, N. (2006) Increased male mating rate in Drosophila associated with Wolbachia infection. Journal of Evolutionary Biology, 19, 1964–1972.Google Scholar
de Roode, JC, Lefèvre, , Hunter, MD. (2013) Self-medication in animals. Science, 340, 150–151.Google Scholar
Degnan, P, Pusey, A, Lonsdorf, E, et al. (2012) Factors associated with the diversification of the gut microbial communities within chimpanzees from Gombe National Park. Proceedings of the National Academy of Sciences, 109, 13034–13039.CrossRefGoogle ScholarPubMed
Denison, RF. (2000) Legume sanctions and the evolution of symbiotic cooperation by rhizobia. The American Naturalist, 156, 567–576.Google Scholar
Desbonnet, L, Garrett, L, Clarke, G, et al. (2010) Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience, 170, 1179–1188.Google Scholar
Desbonnet, L, Clarke, G, Shanahan, F, et al. (2014) Microbiota is essential for social development in the mouse. Molecular Psychiatry, 19, 146–148.CrossRefGoogle ScholarPubMed
Diaz-Heijtz, R, Wang, S, Anuar, F, et al. (2011) Normal gut microbiota modulates brain development and behavior. Proceedings of the National Academy of Sciences, 108, 3047–3052.CrossRefGoogle ScholarPubMed
Dillon, RJ, Vennard, CT, Charnley, AK. (2000) Pheromones: Exploitation of gut bacteria in the locust. Nature, 403, 851.Google Scholar
Dillon, RJ, Vennard, CT, Charnley, AK. (2002) A note: Gut bacteria produce components of a locust cohesion pheromone. Journal of Applied Microbiology, 92, 759–763.Google Scholar
Dinan, TG, Cryan, JF. (2012) Regulation of the stress response by the gut microbiota: Implications for psychoneuroendocrinology. Psychoneuroendocrinology, 37, 1369–1378.CrossRefGoogle ScholarPubMed
Dinan, TG, Stanton, C, Cryan, JF. (2013) Psychobiotics: A novel class of psychotropic. Biological Psychiatry, 74, 720–726.Google Scholar
Dinan, TG, Stilling, RM, Stanton, C, et al. (2015) Collective unconscious: How gut microbes shape human behavior. Journal of Psychiatric Research, 63, 1–9.Google Scholar
Dodd, DMB. (1989) Reproductive isolation as a consequence of adaptive divergence in Drosophila pseudoobscura. Evolution, 43, 1308–1311.Google Scholar
Dunn, AM, Andrews, T, Ingrey, H, et al. (2006) Strategic sperm allocation under parasitic sex-ratio distortion. Biology Letters, 2, 78–80.CrossRefGoogle ScholarPubMed
Dyson, EA, Hurst, GDD. 2004. Persistence of an extreme sex-ratio bias in a natural population. Proceedings of the National Academy of Sciences, 101, 6520–6523.Google Scholar
Elgart, M, Stern, S, Salton, O, et al. (2016) Impact of gut microbiota on the fly’s germ line. Nature Communications, 7, 11280.Google Scholar
Engelstädter, J, Hurst, GDD. (2009) The ecology and evolution of microbes that manipulate host reproduction. Annual Review of Ecology and Systematics, 40, 127–149.Google Scholar
Erkosar, B, Storelli, G, Mitchell, M, et al. (2015) Pathogen virulence impedes mutualist-mediated enhancement of host juvenile growth via inhibition of protein digestion. Cell Host Microbe, 18, 445–455.Google Scholar
Evans, O, Caragata, EP, McMeniman, CJ, et al. (2009) Increased locomotor activity and metabolism of Aedes aegypti infected with a life-shortening strain of Wolbachia pipientis. Journal of Experimental Biology, 212, 1436–1441.Google Scholar
Ezenwa, VO, Gerardo, NM, Inouye, DW, et al. (2012) Animal behavior and the microbiome. Science, 338, 198–199.CrossRefGoogle ScholarPubMed
Ezenwa, VO, Williams, AE. (2014) Microbes and animal olfactory communication: Where do we go from here? BioEssays, 36, 847–854.Google Scholar
Falik, O, Mordoch, Y, Quansah, L, et al. (2011) Rumor has it …: Relay communication of stress cues in plants. PLoS ONE, 6, e23625.Google Scholar
Farine, JP, Habbachi, W, Cortot, J, et al. (2017) Maternally-transmitted microbiota affects odor emission and preference in Drosophila larva. Scientific Reports, 7, 6062.Google Scholar
Fernandez-Real, JM, Serino, M, Blasco, G, et al. (2015) Gut microbiota interacts with brain microstructure and function. The Journal of Clinical Endocrinology & Metabolism, 100, 4505–4513.Google Scholar
Ferveur, JF, Cobb, M. (2010) Behavioral and evolutionary roles of cuticular hydrocarbons in Diptera. In: Blomqvist, GJ, Bagnères, AG. (Eds.) Insect Hydrocarbons. Cambridge: Cambridge University Press.Google Scholar
Fleury, F, Vavre, F, Ris, N, et al. (2000) Physiological cost induced by the maternally-transmitted endosymbiont Wolbachia in the Drosophila parasitoid Leptopilina heterotoma. Parasitology, 121, 493–500.Google Scholar
Flores, R, Shi, J, Fuhrman, B, et al. (2012) Fecal microbial determinants of fecal and systemic estrogens and estrogen metabolites: A cross-sectional study. Journal of Translational Medicine, 10, 1–11.Google Scholar
Forbey, JS, Harvey, AL, Huffman, MA, et al. (2009) Exploitation of secondary metabolites by animals: A response to homeostatic challenges. Integrative and Comparative Biology, 49, 314–328.CrossRefGoogle ScholarPubMed
Foster, JA, McVey Neufeld, KA. (2013) Gut–brain axis: How the microbiome influences anxiety and depression. Trends in Neurosciences, 36, 305–312.Google Scholar
Fox, C, Eichelberger, K. (2015) Maternal microbiome and pregnancy outcomes. Fertility and Sterility, 104, 1358–1363.Google Scholar
Franasiak, JM, Scott, RT. (2015a) Microbiome in human reproduction. Fertility and Sterility, 104, 1341–1343.Google Scholar
Franasiak, JM, Scott, RT. (2015b) Reproductive tract microbiome in assisted reproductive technologies. Fertility and Sterility, 104, 1364–1371.Google Scholar
Frohlich, EE, Farzi, A, Mayerhofer, R, et al. (2016) Cognitive impairment by antibiotic-induced gut dysbiosis: Analysis of gut microbiota–brain communication. Brain, Behavior, and Immunity, 56, 140–155.Google Scholar
Gareau, MG, Wine, E, Rodrigues, DM, et al. (2011) Bacterial infection causes stress-induced memory dysfunction in mice. Gut, 60, 307–317.CrossRefGoogle ScholarPubMed
Gareau, M. (2014) Microbiota–gut–brain axis and cognitive function. In: Lyte, M, Cryan, J. (Eds.) Microbial Endocrinology: The Microbiota–Gut–Brain Axis in Health and Disease. Advances in Experimental Medicine and Biology. New York, NY: Springer.Google Scholar
Gavriel, S, Jurkevitch, E, Gazit, Y, et al. (2011) Bacterially enriched diet improves sexual performance of sterile male Mediterranean fruit flies. Journal of Applied Entomology, 135, 564–573.Google Scholar
Gegear, RJ, Otterstatter, MC, Thomson, JD. (2006) Bumble-bee foragers infected by a gut parasite have an impaired ability to utilize floral information. Proceedings of the Royal Society B: Biological Sciences, 273, 1073–1078.Google Scholar
Gorman, ML. (1976) A mechanism for individual recognition by odour in Herpestes auropunctatus (Carnivora: Viverridae). Animal Behaviour, 24, 141–145.Google Scholar
Gotah, T, Noda, H, Hong, XY. (2003) Wolbachia distribution and cytoplasmic incompatibility based on a survey of 42 spider mite species (Acari: Tetranychidae) in Japan. Heredity, 91, 208–216.Google Scholar
Goyal, MS, Venkatesh, S, Milbrandt, J, et al. (2015) Feeding the brain and nurturing the mind: Linking nutrition and the gut microbiota to brain development. Proceedings of the National Academy of Sciences, 112, 14105–14112.Google Scholar
Hadley, NF. (1981) Cuticular lipids of terrestrial plants and arthropods: A comparison of their structure, composition, and waterproofing function. Biological Reviews, 56, 23–47.CrossRefGoogle Scholar
Haegeman, A, Vanholme, B, Jacob, J, et al. (2009) An endosymbiotic bacterium in a plant-parasitic nematode: Member of a new Wolbachia supergroup. International Journal for Parasitology, 39, 1045–1054.Google Scholar
Heijtz, RD, Wang, S, Anuar, F, et al. (2011) Normal gut microbiota modulates brain development and behavior. Proceedings of the National Academy of Sciences, 108, 3047–3052.CrossRefGoogle Scholar
Helletsgruber, C, Dӧtterl, S, Ruprecht, U, et al. (2017) Epiphytic bacteria alter floral scent emissions. Journal of Chemical Ecology, 43, 1073–1077.Google Scholar
Heys, C, Lizé, A, Colinet, H, et al. (2018) Evidence that the microbiota counteracts male outbreeding strategy by inhibiting sexual signaling in females. Frontiers in Ecology and Evolution, 6, 29.Google Scholar
Hilgenboecker, K, Hammerstein, P, Schlattmann, P, et al. (2008) How many species are infected with Wolbachia? A statistical analysis of current data. FEMS Microbiology Letters, 281, 215–220.Google Scholar
Hoban, AE, Stilling, RM, Moloney, G, et al. (2018) The microbiome regulates amygdala-dependent fear recall. Molecular Psychiatry, 23, 1134–1144.Google Scholar
Hoffmann, AA, Turelli, M, Simmons, GM. (1986) Unidirectional incompatibility between populations of Drosophila simulans. Evolution, 40, 692–701.Google Scholar
Hoogland, ICM, Houbolt, C, van Westerloo, DJ, et al. (2015) Systemic inflammation and microglial activation: Systematic review of animal experiments. Journal of Neuroinflammation, 12, 114.Google Scholar
Hooper, LV, Littman, DR, Macpherson, AJ. (2012) Interactions between the microbiota and the immune system. Science, 336, 1268–1273.Google Scholar
Hoover, K, Grove, M, Gardner, M, et al. (2011) A gene for an extended phenotype. Science, 333, 1401.Google Scholar
Hortal, S, Plett, KL, Plett, JM, et al. (2017) Role of plant–fungal nutrient trading and host control in determining the competitive success of ectomycorrhizal fungi. The ISME Journal, 11, 2666–2676.CrossRefGoogle ScholarPubMed
Hosokawa, T, Kikuchi, Y, Shimada, M, et al. 2007. Symbiont acquisition alters behaviour of stinkbug nymphs. Biology Letters, 4, 45–48.Google Scholar
Hsiao, EY, McBride, SW, Hsien, S, et al. (2013) Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell, 155, 1451–1463.Google Scholar
Huang, JH, Douglas, AE. (2015) Consumption of dietary sugar by gut bacteria determines Drosophila lipid content. Biology Letters, 11, 20150469.Google Scholar
Hughes, DP, Andersen, SB, Hywel-Jones, NL, et al. (2011) Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. BMC Ecology, 11, 13.Google Scholar
Hughes, DP, Araújo, JPM, Loreto, RG, et al. (2016) From so simple a beginning: The evolution of behavioral manipulation by fungi. In: Lovett, B, St Leger, RJ. (Eds.) Genetics and Molecular Biology of Entomopathogenic Fungi, Advances in Genetics. New York, NY: Academic Press.Google Scholar
Humber, R. (1982) Strongwellsea vs. Erynia: The case for a phylogenetic classification of the Entomophthorales (Zygomycetes). Mycotaxon, 15, 167–184.Google Scholar
Hurst, GDD, Graf von der Schulenburg, JH, Majerus, TM, et al. (1999) Invasion of one insect species, Adalia bipunctata, by two different male-killing bacteria. Insect Molecular Biology, 8, 133–139.Google Scholar
Jeyaprakash, A, Hoy, MA. (2000) Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Molecular Biology, 9, 393–405.Google Scholar
Jiang, PF, Zhu, T, Gao, JD, et al. (2013) The effect of maternal infection on cognitive development and hippocampus neuronal apoptosis, proliferation and differentiation in the neonatal rats. Neuroscience, 246, 422–434.CrossRefGoogle ScholarPubMed
Junker, RR, Keller, A. (2015) Microhabitat heterogeneity across leaves and flower organs promotes bacterial diversity. FEMS Microbiology Ecology, 91, fiv097.Google Scholar
Kamita, SG, Nagasaka, K, Chua, JW, et al. (2005) A baculovirus encoded protein tyrosine phosphatase gene induces enhanced locomotory activity in a lepidopteran host. Proceedings of the National Academy of Sciences, 102, 2584–2589.Google Scholar
Katan, M, Moon, YP, Paik, MC, et al. (2013) Infectious burden and cognitive function: The Northern Manhattan study. Neurology, 80, 1209–1215.Google Scholar
Kau, AL, Ahern, PP, Griffin, NW, et al. (2011) Human nutrition, the gut microbiome, and immune system: Envisioning the future. Nature, 474, 327–336.Google Scholar
Kennedy, PJ, Clarke, G, O’Neill, A, et al. (2014) Cognitive performance in irritable bowel syndrome: Evidence of a stress-related impairment in visuospatial memory. Psychological Medicine, 44, 1553–1566.Google Scholar
Kiers, ET, Duhamel, M, Beesetty, Y, et al. (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science, 333, 880–882.CrossRefGoogle ScholarPubMed
Kishani Farahani, HK, Ashouri, A, Goldansaz, SH, et al. (2017) Decrease of memory retention in a parasitic wasp: An effect of host manipulation by Wolbachia? Insect Science, 24, 569–583.Google Scholar
Krimbas, CB. (1993) Drosophila subobscura: Biology, Genetics and Inversion Polymorphism. Hamburg: Dr Kovac.Google Scholar
Kunc, M, Gabrych, A, Witkowski, JM. (2016) Microbiome impact on metabolism and function of sex, thyroid, growth and parathyroid hormones. Acta Biochimica Polonica, 63, 189–201.Google Scholar
Lam, K, Babor, D, Duthie, B, et al. (2007) Proliferating bacterial symbionts on house fly eggs affect oviposition behaviour of adult flies. Animal Behaviour, 74, 81–92.CrossRefGoogle Scholar
Lee, KP, Cory, JS, Wilson, K, et al. (2006) Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proceedings of the Royal Society B: Biological Sciences, 273, 823–829.Google Scholar
Lee, K, Mylonakis, E. (2017) An intestine-derived neuropeptide controls avoidance behavior in Caenorhabditis elegans. Cell Reports, 20, 2501–2512.Google Scholar
Lefèvre, T, Oliver, L, Hunter, MD, et al. (2010) Evidence for trans-generational medication in nature. Ecology Letters, 13, 1485–1493.Google Scholar
Leftwich, PT, Clarke, NVE, Hutchings, MI, et al. (2017) Gut microbiomes and reproductive isolation in Drosophila. Proceedings of the National Academy of Sciences, 114, 12767–12772.Google Scholar
Leitão-Gonçalves, R, Carvalho-Santos, Z, Francisco, AP, et al. (2017) Commensal bacteria and essential amino acids control food choice behavior and reproduction. PLoS Biology, 15, e2000862.Google Scholar
Ley, RE, Bäckhead, F, Turnbaugh, P, et al. (2005) Obesity alters gut microbial ecology. Proceedings of the National Academy of Sciences, 102, 11070–11075.Google Scholar
Ley, RE, Turnbaugh, PJ, Klein, S, et al. (2006) Microbial ecology: Human gut microbes associated with obesity. Nature, 444, 1022–1023.Google Scholar
Liang, S, Wang, T, Hu, X, et al. (2015) Administration of Lactobacillus helveticus NS8 improves behavioral, cognitive and biochemical aberrations caused by chronic restraints stress. Neuroscience, 310, 561–577.Google Scholar
Libersat, F, Delago, A, Gal, R. (2009) Manipulation of host behavior by parasitic insects and insect parasites. Annual Review of Entomology, 54, 189–207.Google Scholar
Lizé, A, McKay, R, Lewis, Z. (2013) Gut microbiota and kin recognition. Trends in Ecology & Evolution, 28, 325–326.Google Scholar
Lizé, A, McKay, R, Lewis, Z. (2014) Kin recognition in Drosophila: The importance of ecology and gut bacteria. The ISME Journal, 8, 469–477.Google Scholar
Lowry, CA, Smith, DG, Siebler, PH, et al. (2018) The microbiota, immunoregulation, and mental health: Implications for public health. Current Environmental Health Reports, 3, 270–286.Google Scholar
Lu, B, Nagappan, G, Guan, X, et al. (2013) BDNF-based synaptic repair as a disease-modifying strategy for neurodegenerative diseases. Nature Reviews Neuroscience, 14, 401–416.Google Scholar
Lyte, M. (2013) Microbial endocrinology in the microbiome–gut–brain axis: How bacterial production and utilization of neurochemicals influence behavior. PLoS Pathogens, 9, e1003726.Google Scholar
Martin, FM, Uroz, S, Barker, DG. (2017) Ancestral alliances: Plant mutualistic symbiosis with fungi and bacteria. Science, 356, 819.Google Scholar
Matthews, DM, Jenks, SM. (2013) Ingestion of Mycobacterium vaccae decreases anxiety-related behavior and improves learning in mice. Behavioural Processes, 96, 27–35.Google Scholar
Mayer, EA, Knight, R, Mazmanian, SK, et al. (2014) Gut microbes and the brain: Paradigm shift in neuroscience. Journal of Neuroscience, 34, 15490–15496.Google Scholar
McEwen, BS. (2008) Central effects of stress hormones in health and disease: Understanding the protective and damaging effects of stress and stress mediators. European Journal of Pharmacology, 583, 174–185.Google Scholar
Messaoudi, M, Lalonde, R, Violle, N, et al. (2011) Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. British Journal of Nutrition, 105, 755–764.Google Scholar
Miller, W, Ehrman, L, Schneider, D. (2010) Infection speciation revisited: Impact of symbionts-depletion on female fitness and mating behaviour of Drosophila paulistorum. PLoS Pathogens, 6, e1001214.Google Scholar
Miller, EA, Livermore, JA, Alberts, SC, et al. (2017) Ovarian cycling and reproductive state shape the vaginal microbiota in wild baboons. Microbiome, 5, 1–14.Google Scholar
Minkley, N, Fujita, A, Brune, A, et al. (2006) Nest specificity of the bacterial community in termite guts (Hodotermes mossambicus). Insectes Sociaux, 53, 339–344.Google Scholar
Moeller, A, Foerster, S, Wilson, M, et al. (2016) Social behavior shapes the chimpanzee pan-microbiome. Science Advances, 2, e1500997.Google Scholar
Moora, M, Ӧpik, M, Zobel, M. (2004) Performance of two Centaurea species in response to different root-associated microbial communities and to alterations in nutrient availability. Annales Botanici Fennici, 41, 263–271.Google Scholar
Moore, J. (1995) The behavior of parasitized animals. BioScience, 45, 89–96.Google Scholar
Najarro, MA, Sumethasorn, M, Lamoureux, A, et al. (2015) Choosing mates based on the diet of your ancestors: Replication of non-genetic assortative mating in Drosophila melanogaster. PeerJ, 3, e1173.Google Scholar
Neufeld, KM, Kang, N, Bienenstock, J, et al. (2011) Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterology and Motility, 23, 255–264.Google Scholar
Noguera, JC, Aira, M, Pérez-Losada, M, et al. (2018) Glucocorticoids modulate gastrointestinal microbiome in a wild bird. Royal Society Open Science, 5, 171743.Google Scholar
O’Brien, ME, Anderson, H, Kaukel, E, et al. (2004) SRL172 (killed Mycobacterium vaccae) in addition to standard chemotherapy improves quality of life without affecting survival, in patients with advanced non-small-cell lung cancer: Phase III results. Annals of Oncology, 15, 906–914.Google Scholar
O’Neill, SL, Hoffmann, AA, Werren, JH. (1997) Influential Passengers: Inherited Microorganisms and Arthropod Reproduction. Oxford: Oxford University Press.Google Scholar
Ohland, CL, Kish, L, Bell, H, et al. (2013) Effects of Lactobacillus helveticus on murine behavior are dependent on diet and genotype and correlate with alterations in the gut microbiome. Psychoneuroendocrinology, 38, 1738–1747.Google Scholar
Parois, S, Calandreau, L, Kraimi, N, et al. (2017) The influence of a probiotic supplementation on memory in quail suggests a role of gut microbiota on cognitive abilities in birds. Behavioural Brain Research, 331, 47–53.Google Scholar
Peng, Y, Nielsen, JE, Cunningham, JP, et al. (2008) Wolbachia infection alters olfactory-cued locomotion in Drosophila spp. Applied and Environmental Microbiology, 74, 3943–3948.Google Scholar
Pineda, A, Kaplan, I, Bezemer, TM. (2017) Steering soil microbiomes to suppress aboveground insect pests. Trends in Plant Science, 22, 770–778.Google Scholar
Plett, JM, Martin, FM. (2017) Know your enemy, embrace your friend: Using omics to understand how plants respond differently to pathogenic and mutualistic microorganisms. The Plant Journal, 93, 729–746.Google Scholar
Poirotte, C, Kappeler, PM, Ngoubangoye, B, et al. (2016) Morbid attraction to leopard urine in Toxoplasma-infected chimpanzees. Current Biology, 26, 98–99.Google Scholar
Poulin, R. (1995) ‘Adaptive’ changes in the behaviour of parasitized animals: A critical review. International Journal for Parasitology, 25, 1371–1383.Google Scholar
Poulin, R. (2010) Parasite manipulation of host behaviour: An update and frequently asked questions. In: Brockmann, J, Roper, TJ, Naguib, M, et al. (Eds.) Advances in the Study of Behaviour. New York, NY: Academic Press.Google Scholar
Rhoades, DF. (1983) Responses of alder and willow to attack by tent caterpillars and webworms: evidence for pheromonal sensitivity of willows. In: Hedin, PA. (Ed.) Plant Resistance to Insects. Washington, DC: American Chemical Society Symposium Series.Google Scholar
Ridlon, JM, Ikegawa, S, Alves, JMP, et al. (2013) Clostridium scindens: A human gut microbe with a high potential to convert glucocorticoids into androgens. The Journal of Lipid Research, 54, 2437–49.Google Scholar
Roager, HM, Licht, TR. (2018) Microbial tryptophan catabolites in health and disease. Nature Communications, 9, 3294.Google Scholar
Romijn, AR, Rucklidge, JJ. (2015) Systematic review of evidence to support the theory of psychobiotics. Nutrition Reviews, 73, 675–693.Google Scholar
Rosenberg, E, Zilber-Rosenberg, I. (2016) Microbes drive evolution of animals and plants: The hologenome concept. mBio, 7, e01395–15.Google Scholar
Rousseaux, C, Thuru, X, Gelot, A, et al. (2007) Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors. Nature Methods, 13, 35–37.Google Scholar
Rousset, F, Bouchon, D, Pintereau, B, et al. (1992) Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods. Proceedings of the Royal Society B: Biological Sciences, 250, 91–98.Google Scholar
Sachs, JL, Russell, JE, Lii, YE, et al. (2010) Host control over infection and proliferation of a cheater symbiont. Journal of Evolutionary Biology, 23, 1919–1927.Google Scholar
Sampson, TR, Mazmanian, SK. (2015) Control of brain development, function, and behavior by the microbiome. Cell Host Microbe, 17, 565–576.Google Scholar
Sanchez, MI, Ponton, F, Schmidt-Rhaesa, A, et al. (2008) Two steps to suicide in crickets harbouring hairworms. Animal Behaviour, 76, 1621–1624.Google Scholar
Sandrini, S, Aldriwesh, M, Alruways, M, et al. (2015) Microbial endocrinology: Host–bacteria communication within the gut microbiome. Journal of Endocrinology 225, R21–R34.CrossRefGoogle ScholarPubMed
Sarkar, A, Lehto, SM, Harty, S, et al. (2016) Psychobiotics and the manipulation of bacteria–gut–brain signals. Trends in Neurosciences, 39, 763–781.Google Scholar
Savignac, HM, Kiely, B, Dinan, TG, et al. (2014) Bifidobacteria exert strain-specific effects on stress-related behaviour and physiology in BALB/c mice. Neurogastroenterology and Motility, 26, 1615–1627.Google Scholar
Savignac, HM, Tramullas, M, Kiely, B, et al. (2015) Bifidobacteria modulate cognitive processes in an anxious mouse strain. Behavioural Brain Research, 287, 59–72.Google Scholar
Schwarzer, M, Makki, K, Storelli, G, et al. (2016) Lactobacillus plantarum strain maintains growth of infant mice during chronic undernutrition. Science, 351, 854–857.Google Scholar
Sharon, G, Garg, N, Debelius, J, et al. (2014) Specialized metabolites from the microbiome in health and disease. Cell Metabolism, 20, 719–730.Google Scholar
Sharon, G, Segal, D, Ringo, JM, et al. (2010) Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proceedings of the National Academy of Sciences, 107, 20051–20056.Google Scholar
Shin, SC, Kim, S-H, You, H, et al. (2011) Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science, 334, 670–674.Google Scholar
Shropshire, JD, Bordenstein, SR. (2016) Speciation by symbiosis: The microbiome and behaviour. mBio, 7, e01785–15.Google Scholar
Simpson, SJ, Raubenheimer, D. (2012) The Nature of Nutrition. Princeton, NJ: Princeton University Press.Google Scholar
Sin, YW, Buesching, CD, Burke, T, et al. (2012) Molecular characterization of the microbial communities in the subcaudal gland secretion of the European badger (Meles meles). FEMS Microbiology Ecology, 81, 648–659.Google Scholar
Smith, MI, Yatsunenko, T, Manary, MJ, et al. (2013) Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science, 339, 548–554.Google Scholar
Soderholm, JD, Yang, PC, Ceponis, P, et al. (2002) Chronic stress induces mast cell-dependent bacterial adherence and initiates mucosal inflammation in rat intestine. Gastroenterology, 123, 1099–1108.Google Scholar
Soper, RS. (1963) Massospora laevispora, a new species of fungus pathogenic to the cicada, Okanagana rimosa. Revue Canadienne de Botanique, 41, 875–878.Google Scholar
Soper, RS, Delyzer, AJ, Smith, FLR. (1976) The genus Massospora, entomopathogenic for cicadas. Part. II. Biology of Massospora levispora and its host Okanagana rimosa, with notes on Massospora cicadina on the periodical cicadas. Annals of the Entomological Society of America, 69, 88–95.Google Scholar
Steiger, S. (2012) New synthesis – Visual and chemical ornaments: What researchers of signal modalities can learn from each other. Journal of Chemical Ecology, 38, 1.Google Scholar
Stilling, RM, Moloney, GM, Ryan, FJ, et al. (2018) Social interaction-induced activation of RNA splicing in the amygdala of microbiome-deficient mice. eLife, 7, e33070.Google Scholar
Storelli, G, Defaye, A, Erkosar, B, et al. (2011) Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metabolism, 14, 403–414.Google Scholar
Stothart, MR, Bobbie, CB, Schulte-Hostedde, AI, et al. (2016) Stress and the microbiome: Linking glucocorticoids to bacterial community dynamics in wild red squirrels. Biology Letters, 12, 2016–2019.Google Scholar
Stouthamer, R, Breeuwer, JA, Hurst, GDD. (1999) Wolbachia pipientis: Microbial manipulator of arthropod reproduction. Annual Review of Microbiology, 53, 71–102.Google Scholar
Stouthamer, R, Luck, RE, Hamilton, WD. (1990) Antibiotics cause parthenogenetic Trichogramma (Hymenoptera: Trichogrammatidae) to revert to sex. Proceedings of the National Academy of Sciences, 87, 2424–2427.Google Scholar
Subramanian, S, Blanton, LV, Frese, SA, et al. (2015) Cultivating healthy growth and nutrition through the gut microbiota. Cell, 161, 36–48.Google Scholar
Sudo, N. (2014) Microbiome, HPA axis and production of endocrine hormones in the gut. In: Lyte, M, Cryan, J. (Eds.) Microbial Endocrinology: The Microbiota–Gut–Brain Axis in Health and Disease. Advances in Experimental Medicine and Biology. New York, NY: Springer.Google Scholar
Swartz, T, Duca, F, de Wouters, T, et al. (2012) Up-regulation of intestinal type 1 taste receptor 3 and sodium glucose luminal transporter-1 expression and increased sucrose intake in mice lacking gut microbiota. British Journal of Nutrition, 107, 621–630.Google Scholar
Theis, KR, Schmidt, TM, Holekamp, KE. (2012) Evidence for a bacterial mechanism for group-specific social odors among hyenas. Scientific Reports, 2, 615.Google Scholar
Theis, KR, Venkataraman, A, Dycus, JA, et al. (2013) Symbiotic bacteria appear to mediate hyena social signals. Proceedings of the National Academy of Sciences, 110, 19832–19837.Google Scholar
Thomas, F, Schmidt-Rhaesa, A, Martin, G, et al. (2002) Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts? Journal of Evolutionary Biology, 15, 356–361.Google Scholar
Trewavas, A. (2009) What is plant behaviour? Plant, Cell & Environment, 32, 606–616.Google Scholar
Trewavas, A. (2017) The foundations of plant intelligence. Interface Focus, 7, 20160098.Google Scholar
Tung, J, Barreiro, L, Burns, M, et al. (2015) Social networks predict gut microbiome composition in wild baboons. eLife, 4, e05224.Google Scholar
Turnbaugh, PJ, Ley, RE, Mahowald, MA, et al. (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature, 444, 1027–1131.Google Scholar
Turnbaugh, PJ, Hamady, M, Yatsunenko, T, et al. (2009) A core gut microbiome in obese and lean twins. Nature, 457, 480–484.Google Scholar
Vala, F, Egas, M, Breeuwer, JAJ, et al. (2004) Wolbachia affects oviposition and mating behaviour of its spider mite host. Journal of Evolutionary Biology, 17, 692–700.CrossRefGoogle ScholarPubMed
Vandenkoornhuyse, P, Quaiser, A, Duhamel, M, et al. (2015) The importance of the microbiome of the plant holobiont. New Phytologist, 206, 1196–1206.Google Scholar
Venu, I, Durisko, Z, Xu, J, et al. (2014) Social attraction mediated by fruit flies’ microbiome. Journal of Experimental Biology, 217, 1346–1352.Google Scholar
Vijay-Kumar, M, Aitken, JD, Carvalho, FA, et al. (2010) Metabolic syndrome and altered gut microbiota in mice lacking toll-like receptor 5. Science, 328, 228–231.Google Scholar
Vlčková, K, Shutt-Phillips, K, Heistermann, M, et al. (2018) Impact of stress on the gut microbiome of free-ranging western lowland gorillas. Microbiology, 164, 40–44.Google Scholar
Vuong, HE, Yano, JM, Fung, TC, et al. (2017) The microbiome and host behavior. Annual Review of Neuroscience, 40, 21–49.Google Scholar
Wada-Katsumata, A, Zurek, L, Nalyanya, G, et al. (2015) Gut bacteria mediate aggregation in the German cockroach. Proceedings of the National Academy of Sciences, 112, 15678–15683.Google Scholar
Wall, R, Cryan, JF, Ross, RP, et al. (2014) Bacterial neuroactive compounds produced by psychobiotics. Advances in Experimental Medicine and Biology, 817, 221–239.Google Scholar
Walsh, BS, Heys, C, Lewis, Z. (2017) Gut microbiota influences female choice and fecundity in the nuptial gift-giving species, Drosophila subobscura (Diptera: Drosophilidae). European Journal of Entomology, 114, 439–445.Google Scholar
Wang, T, Hu, X, Liang, S, et al. (2015) Lactobacillus fermentum NS9 restores the antibiotic induced physiological and psychological abnormalities in rats. Beneficial Microbes, 6, 707–717.Google Scholar
Werner, GDA, Cornwell, WK, Sprent, JI, et al. (2014) A single evolutionary innovation drives the deep evolution of symbiotic N2 fixation in angiosperms. Nature Communications, 5, 4087.Google Scholar
Werren, JH, Baldo, L, Clark, ME. (2008) Wolbachia: Master manipulators of invertebrate biology. Nature Reviews Microbiology, 6, 741–751.Google Scholar
Witting, PA. (1979) Learning capacity and memory of normal and Toxoplasma-infected laboratory rats and mice. Zeitschrift fur Parasitenkunde, 61, 29–51.Google Scholar
Wong, CNA, Ng, P, Douglas, AE. (2011) Low‐diversity bacterial community in the gut of the fruit fly Drosophila melanogaster. Environmental Microbiology, 13, 1889–1900.Google Scholar
Wong, AC-N, Holmes, A, Ponton, F, et al. (2015) Behavioral microbiomics: A multi-dimensional approach to microbial influence on behavior. Frontiers in Microbiology, 6, 1359.Google Scholar
Wong, AC-N, Wang, Q-P, Morimoto, J, et al. (2017) Gut microbiota modifies olfactory-guided microbial preferences and foraging decisions in Drosophila. Current Biology, 27, 2397–2404.Google Scholar
Wyatt, TD. (2014) Pheromones and Animal Behaviour: Chemical Signals and Signature Mixes. Cambridge: Cambridge University Press.Google Scholar
Yamada, R, Deshpande, SA, Bruce, KD, et al. (2015) Microbes promote amino acid harvest to rescue undernutrition in Drosophila. Cell Reports, 10, 865–872.Google Scholar
Zareie, M, Johnson-Henry, K, Jury, J, et al. (2006) Probiotics prevent bacterial translocation and improve intestinal barrier function in rats following chronic psychological stress. Gut, 55, 1553–1560.Google Scholar
Zhang, Y, Lu, H, Bargmann, CI. (2005) Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature, 438, 179–184.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×