Behavioral Microbiomics: A Multi-Dimensional Approach to Microbial Influence on Behavior
Open accessAbstract
The role of microbes as a part of animal systems has historically been an under-appreciated aspect of animal life histories. Recently, evidence has emerged that microbes have wide-ranging influences on animal behavior. Elucidating the complex relationships between host-microbe interactions and behavior requires an expanded ecological perspective, involving the host, the microbiome and the environment; which, in combination, is termed the holobiont. We begin by seeking insights from the literature on host-parasite interactions, then expand to consider networks of interactions between members of the microbial community. A central aspect of the environment is host nutrition. We describe how interactions between the nutrient environment, the metabolic and behavioral responses of the host and the microbiome can be studied using an integrative framework called nutritional geometry, which integrates and maps multiple aspects of the host and microbial response in multidimensional nutrient intake spaces.
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Gut microbiota influences the development of social behavior.
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From Autism, Gastrointestinal Symptoms and Modulation of Gut Microbiota by Nutritional Interventions (2019) · cites this paper as [164]
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Duca, F. A., Sakar, Y., Lepage, P., Devime, F., Goustard, B., Dore, J. M., & Covașă, M. (2014) · Diabetes · doi:10.2337/db13-1526 · Cited by 162 · see citing works
RetractedAn obesity-associated gut microbiome with increased capacity for energy harvest
Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., Magrini, V., Mardis, E. R., & Gordon, J. I. (2006) · Nature · doi:10.1038/nature05414 · Cited by 12,444 · see citing works
Ng, M., Fleming, T., Robinson, M., Thomson, B., Graetz, N., Margono, C., Mullany, E. C., Biryukov, S., Abbafati, C., Abera, S. F., et al. (2014) · The Lancet · doi:10.1016/s0140-6736(14)60460-8 · Cited by 11,952 · see citing works
Sakurai, T., Amemiya, A., Ishii, M., Matsuzaki, I., Chemelli, R. M., Tanaka, H., Williams, S. C., Richardson, J. A., Kozlowski, G. P., Wilson, S., et al. (1998) · Cell · doi:10.1016/s0092-8674(00)80949-6 · Cited by 5,501 · see citing works
The gut microbiota shapes intestinal immune responses during health and disease
Round, J. L., & Mazmanian, S. K. (2009) · Nature Reviews Immunology · doi:10.1038/nri2515 · Cited by 5,029 · see citing works
Prokaryotes: The unseen majority
Whitman, W. B., Coleman, D. C., & Wiebe, W. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.12.6578 · Cited by 4,871 · cited 4× · see citing works
“…in Microbiology Received: 24 June 2015 Accepted: 16 November 2015 Published: 27 November 2015 Citation: Wong AC-N, Holmes A, Ponton F, Lihoreau M, Wilson K, Raubenheimer D and Simpson SJ (2015) Behavioral Microbiomics: A Multi-Dimensional Approach to Microbial Influence on Behavior.”
BackgroundInfluentialHost-gut microbiota metabolic interactions
Nicholson, J. K., Holmes, E., Kinross, J., Burcelin, R., Gibson, G., Jia, W., & Pettersson, S. (2012) · Science · doi:10.1126/science.1223813 · Cited by 4,760 · see citing works
Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour
Cryan, J. F., & Dinan, T. G. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3346 · Cited by 4,572 · see citing works
Bravo, J. A., Forsythe, P., Chew, M. V., Escaravage, E., Savignac, H. M., Dinan, T. G., Bienenstock, J., & Cryan, J. F. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102999108 · Cited by 3,888 · see citing works
Ecological and Evolutionary Forces Shaping Microbial Diversity in the Human Intestine
Ley, R. E., Peterson, D. A., & Gordon, J. I. (2006) · Cell · doi:10.1016/j.cell.2006.02.017 · Cited by 3,358 · see citing works
Hsiao, E. Y., McBride, S. W., Hsien, S., Sharon, G., Hyde, E. R., McCue, T., Codelli, J. A., Chow, J., Reisman, S. E., Petrosino, J. F., et al. (2013) · Cell · doi:10.1016/j.cell.2013.11.024 · Cited by 3,283 · see citing works
Normal gut microbiota modulates brain development and behavior
Heijtz, R. D., Wang, S., Anuar, F., Qian, Y., Björkholm, B., Samuelsson, A., Hibberd, M. L., Forssberg, H., & Pettersson, S. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010529108 · Cited by 3,228 · see citing works
Sudo, N., Chida, Y., Aiba, Y., Sonoda, J., Oyama, N., Yu, X., Kubo, C., & Koga, Y. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.063388 · Cited by 2,735 · see citing works
Dietary modulation of the human colonic microbiota: updating the concept of prebiotics
Gibson, G. R., Probert, H. M., Loo, J. V., Rastall, R. A., & Roberfroid, M. B. (2004) · Nutrition Research Reviews · doi:10.1079/nrr200479 · Cited by 2,539 · see citing works
The role of short chain fatty acids in health and disease
Tan, J., McKenzie, C., Potamitis, M., Thorburn, A. N., Mackay, C. R., & Macia, L. (2014) · Advances in immunology · doi:10.1016/b978-0-12-800100-4.00003-9 · Cited by 2,425 · see citing works
Arms races between and within species
Dawkins, R., & Krebs, J. R. (1979) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1979.0081 · Cited by 2,163 · see citing works
Bercik, P., Denou, E., Collins, J., Jackson, W., Lu, J., Jury, J., Deng, Y., Blennerhassett, P., Macri, J., McCoy, K. D., et al. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.04.052 · Cited by 1,748 · see citing works
Bacteria as vitamin suppliers to their host: A gut microbiota perspective
LeBlanc, J. G., Milani, C., de Giori, G. S., Sesma, F., van Sinderen, D., & Ventura, M. (2013) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2012.08.005 · Cited by 1,613 · see citing works
Reciprocal interactions of the intestinal microbiota and immune system
Maynard, C. L., Elson, C. O., Hatton, R. D., & Weaver, C. T. (2012) · Nature · doi:10.1038/nature11551 · Cited by 1,598 · cited 2× · see citing works
“…tissue development (Stappenbeck et al., 2002), nutrient absorption (Gibson et al., 2004; Turnbaugh et al., 2006), immunity (Round andMazmanian, 2009;Maynard et al., 2012), and circadian regulation (Thaiss et al., 2014; Zarrinpar et al., 2014; Leone et al., 2015) are emergent properties of the…”
BackgroundSamuel, B. S., Shaito, A., Motoike, T., Rey, F. E., Backhed, F., Manchester, J. K., Hammer, R. E., Williams, S. C., Crowley, J., Yanagisawa, M., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808567105 · Cited by 1,564 · see citing works
Transkingdom Control of Microbiota Diurnal Oscillations Promotes Metabolic Homeostasis
Thaiss, C. A., Zeevi, D., Levy, M., Zilberman-Schapira, G., Suez, J., Tengeler, A. C., Abramson, L., Katz, M. N., Korem, T., Zmora, N., et al. (2014) · Cell · doi:10.1016/j.cell.2014.09.048 · Cited by 1,449 · see citing works
Diversity and distribution of coral-associated bacteria
Rohwer, F., Seguritan, V, Azam, F., & Knowlton, N. (2002) · Marine Ecology Progress Series · doi:10.3354/meps243001 · Cited by 1,337 · see citing works
An international association between Helicobacter pylori infection and gastric cancer
The EUROGAST Study Group (1993) · The Lancet · doi:10.1016/0140-6736(93)90938-d · Cited by 1,158 · see citing works
γ-Aminobutyric acid production by culturable bacteria from the human intestine
Barrett, E., Ross, R. P., O'Toole, P. W., Fitzgerald, G. F., & Stanton, C. (2012) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2012.05344.x · Cited by 1,156 · see citing works
Wolbachia and Virus Protection in Insects
Hedges, L. M., Jeremy, B., O’Neill, S. L., & Johnson, K. N. (2008) · Science · doi:10.1126/science.1162418 · Cited by 1,111 · see citing works
Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells
Stappenbeck, T. S., Hooper, L. V., & Gordon, J. I. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.202604299 · Cited by 1,095 · see citing works
Hemarajata, P., & Versalovic, J. (2013) · Therapeutic Advances in Gastroenterology · doi:10.1177/1756283x12459294 · Cited by 1,083 · see citing works
Lifespan and reproduction in <i>Drosophila</i> : New insights from nutritional geometry
Lee, K. P., Simpson, S. J., Clissold, F. J., Brooks, R., Ballard, J. W. O., Taylor, P. W., Soran, N., & Raubenheimer, D. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710787105 · Cited by 1,032 · see citing works
A diversity profile of the human skin microbiotaPreprint
Grice, E. A., Kong, H. H., Renaud, G., Young, A., Bouffard, G. G., Blakesley, R. W., Wolfsberg, T. G., Turner, M. L. C., & Segre, J. A. (2008) · Genome Research · doi:10.1101/gr.075549.107 · Cited by 1,026 · see citing works
Cremer, S., Armitage, S. A. O., & Schmid‐Hempel, P. (2007) · Current Biology · doi:10.1016/j.cub.2007.06.008 · Cited by 1,004 · see citing works
Alexander, G. M., Rogan, S. C., Abbas, A. I., Armbruster, B. N., Pei, Y., Allen, J., Nonneman, R. J., Hartmann, J. F., Moy, S. S., Nicolelis, M. A. L., et al. (2009) · Neuron · doi:10.1016/j.neuron.2009.06.014 · Cited by 996 · see citing works
Diet and feeding pattern affect the diurnal dynamics of the gut microbiome
Zarrinpar, A., Chaix, A., Yooseph, S., & Panda, S. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.11.008 · Cited by 926 · see citing works
Leone, V., Gibbons, S. M., Martinez, K., Hutchison, A. L., Huang, E. Y., Cham, C. M., Pierre, J. F., Heneghan, A. F., Nadimpalli, A., Hubert, N., et al. (2015) · Cell Host & Microbe · doi:10.1016/j.chom.2015.03.006 · Cited by 908 · see citing works
Solon-Biet, S. M., McMahon, A. C., Ballard, J. W. O., Ruohonen, K., Wu, L. E., Cogger, V. C., Warren, A., Huang, X., Pichaud, N., Melvin, R. G., et al. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.02.009 · Cited by 904 · see citing works
Gut microbiome, obesity, and metabolic dysfunction
Tilg, H., & Kaser, A. (2011) · Journal of Clinical Investigation · doi:10.1172/jci58109 · Cited by 860 · see citing works
The microbial dimension in insect nutritional ecology
Douglas, A. E. (2009) · Functional Ecology · doi:10.1111/j.1365-2435.2008.01442.x · Cited by 846 · see citing works
Socially transmitted gut microbiota protect bumble bees against an intestinal parasite
Koch, H., & Schmid‐Hempel, P. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1110474108 · Cited by 828 · see citing works
Commensal bacteria play a role in mating preference of Drosophila melanogaster
Sharon, G., Segal, D., Ringo, J. M., Hefetz, A., Zilber‐Rosenberg, I., & ROSENBERG, E. B. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1009906107 · Cited by 825 · see citing works
The role of microbiome in central nervous system disorders
Wang, Y., & Kasper, L. H. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.12.015 · Cited by 803 · see citing works
Fatal attraction in rats infected with Toxoplasma gondii
Berdoy, M., Webster, J. P., & Macdonald, D. W. (2000) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2000.1182 · Cited by 731 · see citing works
The Coral Probiotic Hypothesis
Reshef, L., Koren, O., Loya, Y., Zilber‐Rosenberg, I., & ROSENBERG, E. B. (2006) · Environmental Microbiology · doi:10.1111/j.1462-2920.2006.01148.x · Cited by 707 · see citing works
High-fat diet alters gut microbiota physiology in mice
Daniel, H., Gholami, A. M., Berry, D., Desmarchelier, C., Hahne, H., Loh, G., Mondot, S., Lepage, P., Rothballer, M., Walker, A., et al. (2013) · The ISME Journal · doi:10.1038/ismej.2013.155 · Cited by 680 · see citing works
Simpson, S. J., & Raubenheimer, D. (2012) · Princeton University Press eBooks · doi:10.1515/9781400842803 · Cited by 599 · see citing works
Vyas, A., Kim, S.-K., Giacomini, N., Boothroyd, J. C., & Sapolsky, R. M. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608310104 · Cited by 571 · see citing works
Animal Behavior and the Microbiome
Ezenwa, V. O., Gerardo, N. M., Inouye, D. W., Medina, M., & Xavier, J. B. (2012) · Science · doi:10.1126/science.1227412 · Cited by 524 · see citing works
Exploring host–microbiota interactions in animal models and humansPreprint
Kostic, A. D., Howitt, M. R., & Garrett, W. S. (2013) · Genes & Development · doi:10.1101/gad.212522.112 · Cited by 491 · see citing works
Arnold, I. C., Dehzad, N., Reuter, S., Martin, H., Becher, B., Taube, C., & Mueller, A. (2011) · Journal of Clinical Investigation · doi:10.1172/jci45041 · Cited by 463 · see citing works
Genomewide Association Studies: History, Rationale, and Prospects for Psychiatric Disorders
Psychiatric GWAS Consortium Coordinating Committee (2009) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2008.08091354 · Cited by 450 · see citing works
Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar
Lee, K. P., Cory, J. S., Wilson, K. L., Raubenheimer, D., & Simpson, S. J. (2005) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2005.3385 · Cited by 418 · see citing works
The causes of intestinal dysbiosis: a review.
Hawrelak, J. A., & Myers, S. P. (2004) · PubMed · Cited by 368 · see citing works
Helicobacter pyloriColonization Is Inversely Associated with Childhood Asthma
Chen, Y., & Blaser, M. J. (2008) · The Journal of Infectious Diseases · doi:10.1086/590158 · Cited by 362 · see citing works
MHC-correlated mate choice in humans: A review
Havlı́ček, J., & Roberts, S. C. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.10.007 · Cited by 340 · see citing works
Palmnäs, M. S. A., Cowan, T., Bomhof, M. R., Su, J., Reimer, R. A., Vogel, H. J., Hittel, D. S., & Shearer, J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0109841 · Cited by 337 · see citing works
Modelling the ecological niche from functional traits
Kearney, M., Simpson, S. J., Raubenheimer, D., & Helmuth, B. S. T. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0034 · Cited by 336 · see citing works
Parasitic castration: the evolution and ecology of body snatchers
Lafferty, K. D., & Kuris, A. M. (2009) · Trends in Parasitology · doi:10.1016/j.pt.2009.09.003 · Cited by 310 · see citing works
Singer, M. S., Mace, K. C., & Bernays, E. A. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004796 · Cited by 287 · see citing works
Regulation of myocardial ketone body metabolism by the gut microbiota during nutrient deprivation
Crawford, P. A., Crowley, J. R., Sambandam, N., Muegge, B. D., Costello, E. K., Hamady, M., Knight, R., & Gordon, J. I. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902366106 · Cited by 278 · see citing works
(1993) · PubMed · Cited by 276 · see citing works
Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection
Hughes, D. P., Andersen, S. B., Hywel‐Jones, N. L., Himaman, W., BILLEN, J. P. J., & Boomsma, J. J. (2011) · BMC Ecology · doi:10.1186/1472-6785-11-13 · Cited by 267 · see citing works
fields: Tools for Spatial Data
Nychka, D. W., Furrer, R., Paige, J., Sain, S. R., Gerber, F., Iverson, M., & Johnson, R. (2001) · doi:10.32614/cran.package.fields · Cited by 258 · see citing works
Amoeboid organism solves complex nutritional challenges
Dussutour, A., Latty, T. M., Beekman, M., & Simpson, S. J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0912198107 · Cited by 257 · see citing works
Testing Protein Leverage in Lean Humans: A Randomised Controlled Experimental Study
Gosby, A. K., Conigrave, A. D., Lau, N. S., Iglesias, M. A., Hall, R. M., Jebb, S. A., Brand-Miller, J. C., Caterson, I. D., Raubenheimer, D., & Simpson, S. J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025929 · Cited by 254 · see citing works
Lessons from Studying Insect Symbioses
Douglas, A. E. (2011) · Cell Host & Microbe · doi:10.1016/j.chom.2011.09.001 · Cited by 242 · see citing works
Starks, P. T. B., Blackie, C. A., & Seeley, T. D. (2000) · Die Naturwissenschaften · doi:10.1007/s001140050709 · Cited by 241 · see citing works
Exploitation of gut bacteria in the locust
Dillon, R. J., Vennard, C. T., & Charnley, A. K. (2000) · Nature · doi:10.1038/35002669 · Cited by 229 · see citing works
Moribund Ants Leave Their Nests to Die in Social Isolation
Heınze, J., & Walter, B. (2010) · Current Biology · doi:10.1016/j.cub.2009.12.031 · Cited by 224 · see citing works
Conflict, cheats and the persistence of symbioses
Douglas, A. E. (2008) · New Phytologist · doi:10.1111/j.1469-8137.2007.02326.x · Cited by 217 · see citing works
Penn, D. J., & Potts, W. K. (1998) · Advances in immunology · doi:10.1016/s0065-2776(08)60612-4 · Cited by 205 · see citing works
Access to mutualistic endosymbiotic microbes: an underappreciated benefit of group living
Lombardo, M. P. (2007) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-007-0428-9 · Cited by 189 · see citing works
Putting the Balance Back in Diet
Simpson, S. J., Couteur, D. G. L., & Raubenheimer, D. (2015) · Cell · doi:10.1016/j.cell.2015.02.033 · Cited by 183 · see citing works
Parasites: evolution’s neurobiologists
Adamo, S. A. (2012) · Journal of Experimental Biology · doi:10.1242/jeb.073601 · Cited by 164 · see citing works
Evidence for a bacterial mechanism for group-specific social odors among hyenas
Theis, K. R., Schmidt, T. M., & Holekamp, K. E. (2012) · Scientific Reports · doi:10.1038/srep00615 · Cited by 162 · see citing works
Dynamics of macronutrient self‐medication and illness‐induced anorexia in virally infected insects
Povey, S., Cotter, S. C., Simpson, S. J., & Wilson, K. L. (2013) · Journal of Animal Ecology · doi:10.1111/1365-2656.12127 · Cited by 159 · see citing works
The expression and impact of antifungal grooming in ants
Reber, A., Purcell, J., Buechel, S. D., Buri, P., & Chapuisat, M. (2011) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2011.02230.x · Cited by 149 · see citing works
Dass, S. A. H., & Vyas, A. (2014) · Molecular Ecology · doi:10.1111/mec.12888 · Cited by 145 · see citing works
Parasitic Stress and Self-Medication in Wild Animals
Lozano, G. A. (1998) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)60367-8 · Cited by 143 · see citing works
New paradigms for the evolution of beneficial infections
Sachs, J. L., Essenberg, C. J., & Turcotte, M. M. (2011) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2011.01.010 · Cited by 140 · see citing works
Partner choice and fidelity stabilize coevolution in a Cretaceous-age defensive symbiosis
Kaltenpoth, M., Roeser-Mueller, K., Koehler, S., Peterson, A., Nechitaylo, T. Y., Stubblefield, J. W., Herzner, G., Seger, J., & Strohm, E. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400457111 · Cited by 136 · see citing works
Modelling nutritional interactions: from individuals to communities
Simpson, S. J., Raubenheimer, D., Charleston, M., & Clissold, F. J. (2009) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2009.06.012 · Cited by 126 · see citing works
Lihoreau, M., Buhl, C., Charleston, M., Sword, G. A., Raubenheimer, D., & Simpson, S. J. (2015) · Ecology Letters · doi:10.1111/ele.12406 · Cited by 119 · see citing works
Social attraction mediated by fruit flies' microbiome
Venu, I., Durisko, Z., Xu, J., & Dukas, R. (2014) · Journal of Experimental Biology · doi:10.1242/jeb.099648 · Cited by 114 · see citing works
Osawa, R., Blanshard, W., & O'Callaghan, P. (1993) · Australian Journal of Zoology · doi:10.1071/zo9930611 · Cited by 111 · see citing works
Kin recognition inDrosophila: the importance of ecology and gut microbiota
Lizé, A., McKay, R., & Lewis, Z. (2013) · The ISME Journal · doi:10.1038/ismej.2013.157 · Cited by 106 · see citing works
An overview of parasite-induced behavioral alterations – and some lessons from bats
Moore, J. (2012) · Journal of Experimental Biology · doi:10.1242/jeb.074088 · Cited by 96 · see citing works
Unveiling the mechanism by which microsporidian parasites prevent locust swarm behavior
Shi, W., Guo, Y., Xu, C., Tan, S., Miao, J., Feng, Y., Zhao, H. G., Leger, R. J. S., & Fang, W. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1314009111 · Cited by 95 · see citing works
Symbiont acquisition alters behaviour of stinkbug nymphs
Hosokawa, T., Kikuchi, Y., Shimada, M., & Fukatsu, T. (2007) · Biology Letters · doi:10.1098/rsbl.2007.0510 · Cited by 92 · see citing works
Macronutrients mediate the functional relationship between Drosophila and Wolbachia
Ponton, F., Wilson, K. L., Holmes, A. J., Raubenheimer, D., Robinson, K. L., & Simpson, S. J. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2014.2029 · Cited by 92 · see citing works
Hosts use altered macronutrient intake to circumvent parasite-induced reduction in fecundity
Ponton, F., Lalubin, F., Fromont, C., Wilson, K. L., Behm, C. A., & Simpson, S. J. (2010) · International Journal for Parasitology · doi:10.1016/j.ijpara.2010.06.007 · Cited by 89 · see citing works
Fitness costs associated with mounting a social immune response
Cotter, S. C., Topham, E., Price, A. J., & Kilner, R. M. (2010) · Ecology Letters · doi:10.1111/j.1461-0248.2010.01500.x · Cited by 87 · see citing works
Nutritional PharmEcology: Doses, nutrients, toxins, and medicines
Raubenheimer, D., & Simpson, S. J. (2009) · Integrative and Comparative Biology · doi:10.1093/icb/icp050 · Cited by 81 · see citing works
Kuhn, F., & Natsch, A. (2008) · Journal of The Royal Society Interface · doi:10.1098/rsif.2008.0223 · Cited by 80 · see citing works
Behavioral acquisition of the hindgut fermentation system by hatchling Iguana iguana
Troyer, K. (1984) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00299618 · Cited by 68 · see citing works
Relations hôtes-parasite du trematode Microphallus papillorobustus (Rankin, 1940)
Helluy, S. (1983) · Annales de Parasitologie Humaine et Comparée · doi:10.1051/parasite/1983581001 · Cited by 47 · see citing works
Competitive Advantages of Caedibacter-Infected Paramecia
Kusch, J., Czubatinski, L., Nachname, S., Hübner, M., Alter, M., & Albrecht, P. (2002) · Protist · doi:10.1078/1434-4610-00082 · Cited by 46 · see citing works
Reduced consumption of protein-rich foods follows immune challenge in a polyphagous caterpillar
Mason, P. A., Smilanich, A. M., & Singer, M. S. (2014) · Journal of Experimental Biology · doi:10.1242/jeb.093716 · Cited by 36 · see citing works
Dance, A. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400859111 · Cited by 3 · see citing works
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Why does the microbiome affect behaviour?
Johnson, K. V.-A., & Foster, K. R. (2018) · Nature Reviews Microbiology · doi:10.1038/s41579-018-0014-3 · Cited by 333 · see citing works
Commensal bacteria and essential amino acids control food choice behavior and reproduction
Leitão-Gonçalves, R., Carvalho-Santos, Z., Francisco, A. P., Fioreze, G. T., Anjos, M., Baltazar, C., Elias, A. P., Itskov, P. M., Piper, M. D. W., & Ribeiro, C. (2017) · PLOS Biology · doi:10.1371/journal.pbio.2000862 · Cited by 315 · see citing works
Autism, Gastrointestinal Symptoms and Modulation of Gut Microbiota by Nutritional Interventions
Ristori, M. V., Quagliariello, A., Reddel, S., Ianiro, G., Vicari, S., Gasbarrini, A., & Putignani, L. (2019) · Nutrients · doi:10.3390/nu11112812 · Cited by 214 · see citing works
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Wong, A. C.-N., Wang, Q., Morimoto, J., Senior, A. M., Lihoreau, M., Neely, G. G., Simpson, S. J., & Ponton, F. (2017) · Current Biology · doi:10.1016/j.cub.2017.07.022 · Cited by 209 · see citing works
Microbiome and nutrition in autism spectrum disorder: Current knowledge and research needs
Berding, K., & Donovan, S. M. (2016) · Nutrition Reviews · doi:10.1093/nutrit/nuw048 · Cited by 146 · see citing works
Leulier, F., MacNeil, L. T., Lee, W., Rawls, J. F., Cani, P. D., Schwarzer, M., Zhao, L., & Simpson, S. J. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.02.001 · Cited by 143 · see citing works
The Geometric Framework for Nutrition as a tool in precision medicine
Simpson, S. J., Couteur, D. G. L., James, D. E., George, J., Gunton, J. E., Solon‐Biet, S. M., & Raubenheimer, D. (2017) · Nutrition and Healthy Aging · doi:10.3233/nha-170027 · Cited by 95 · see citing works
Relevance of microbial symbiosis to insect behavior
Hosokawa, T., & Fukatsu, T. (2020) · Current Opinion in Insect Science · doi:10.1016/j.cois.2020.03.004 · Cited by 89 · see citing works
Drosophila females trade off good nutrition with high quality oviposition sites when choosing foods
Lihoreau, M., Poissonnier, L., Isabel, G., & Dussutour, A. (2016) · Journal of Experimental Biology · doi:10.1242/jeb.142257 · Cited by 75 · see citing works
Direct and trans-generational effects of male and female gut microbiota in Drosophila melanogaster
Morimoto, J., Simpson, S. J., & Ponton, F. (2017) · Biology Letters · doi:10.1098/rsbl.2016.0966 · Cited by 66 · see citing works
Akami, M., Ren, X., Qi, X., Mansour, A., Gao, B., Cao, S., & Niu, C. (2019) · BMC Microbiology · doi:10.1186/s12866-019-1607-3 · Cited by 62 · see citing works
The role of insect gut microbiota in host fitness, detoxification and nutrient supplementation
Shamjana, U., Vasu, D. A., Hembrom, P. S., Nayak, K., & Grace, T. (2024) · Antonie van Leeuwenhoek · doi:10.1007/s10482-024-01970-0 · Cited by 57 · see citing works
Towards an Integrative Understanding of Diet–Host–Gut Microbiome Interactions
Read, M. N., & Holmes, A. J. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00538 · Cited by 54 · see citing works
Meloni, M., & Müller, R. (2018) · Current Zoology · doi:10.1093/eep/dvy019 · Cited by 54 · see citing works
Gut bacteria induce oviposition preference through ovipositor recognition in fruit fly
He, M., Chen, H., Yang, X., Gao, Y., Lu, Y., & Cheng, D. (2022) · Communications Biology · doi:10.1038/s42003-022-03947-z · Cited by 49 · see citing works
Effects of parasites and pathogens on bee cognition
Gómez‐Moracho, T., Heeb, P., & Lihoreau, M. (2017) · Ecological Entomology · doi:10.1111/een.12434 · Cited by 49 · see citing works
Heys, C., Lizé, A., Blow, F., White, L. J., Darby, A. C., & Lewis, Z. (2018) · Ecology and Evolution · doi:10.1002/ece3.3991 · Cited by 47 · see citing works
Diabetes and Heart Failure: Multi-Omics Approaches
Tayanloo-Beik, A., Roudsari, P. P., Rezaei–Tavirani, M., Biglar, M., Tabatabaei‐Malazy, O., Arjmand, B., & Larijani, B. A. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.705424 · Cited by 46 · see citing works
Co-niche construction between hosts and symbionts: ideas and evidence
Borges, R. M. (2017) · Journal of Genetics · doi:10.1007/s12041-017-0792-9 · Cited by 44 · see citing works
Hafer, N. (2016) · BioEssays · doi:10.1002/bies.201600060 · Cited by 43 · see citing works
Symbiotic bacteria affect oviposition behavior in the olive fruit fly Bactrocera oleae
Jose, P. A., Ben‐Yosef, M., Jurkevitch, É., & Yuval, B. (2019) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2019.103917 · Cited by 40 · see citing works
Srinivasan, M., Adnane, M., & Archunan, G. (2021) · Research in Veterinary Science · doi:10.1016/j.rvsc.2021.01.003 · Cited by 40 · see citing works
Exploring Interactions between the Gut Microbiota and Social Behavior through Nutrition
Pasquaretta, C., Gómez‐Moracho, T., Heeb, P., & Lihoreau, M. (2018) · Genes · doi:10.3390/genes9110534 · Cited by 31 · see citing works
Robinson, J. M., & Breed, M. F. (2020) · Science of The Total Environment · doi:10.1016/j.scitotenv.2020.137626 · Cited by 30 · see citing works
Boutry, J., Mistral, J., Berlioz, L., Klimovich, A. V., Tökölyi, J., Fontenille, L., Újvári, B., Dujon, A. M., Giraudeau, M., & Frédéric Thomas, A. (2021) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2021.149923 · Cited by 30 · see citing works
Social nutrition: an emerging field in insect science
Lihoreau, M., Gómez‐Moracho, T., Pasquaretta, C., Costa, J. T., & Buhl, C. (2018) · Current Opinion in Insect Science · doi:10.1016/j.cois.2018.05.003 · Cited by 25 · see citing works
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Morimoto, J., & Lihoreau, M. (2019) · The American Naturalist · doi:10.1086/701898 · Cited by 25 · see citing works
The holobiont concept: the case of xylophagous termites and cockroaches
Berlanga, M., & Guerrero, R. (2016) · Symbiosis · doi:10.1007/s13199-016-0388-9 · Cited by 22 · see citing works
Molecular signatures from multi‐omics of autism spectrum disorders and schizophrenia
Nomura, J., Mardo, M., & Takumi, T. (2021) · Journal of Neurochemistry · doi:10.1111/jnc.15514 · Cited by 21 · see citing works
Robinson, J. M., & Cameron, R. W. F. (2020) · Frontiers in Psychology · doi:10.3389/fpsyg.2020.591071 · Cited by 19 · see citing works
Microbial Gatekeepers of Fertility in the Female Reproductive Microbiome of Cattle
Adnane, M., & Chapwanya, A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252010923 · Cited by 16 · see citing works
Changes in diet associated with cancer: An evolutionary perspective
Frédéric Thomas, A., Rome, S., Mery, F., Dawson, E. H., Montagne, J., Biro, P. A., Beckmann, C., François Renaud, A., Poulin, R., Michel Raymond, A., et al. (2017) · Evolutionary Applications · doi:10.1111/eva.12465 · Cited by 15 · see citing works
Personality Affects Zebrafish Response to Sertraline
Shuraiqi, A. A., Abed, R. M. M., Al-Habsi, A. A., & Barry, M. J. (2023) · Environmental Toxicology and Chemistry · doi:10.1002/etc.5769 · Cited by 14 · see citing works
Pignataro, E., Pini, F., Barbanente, A., Arnesano, F., Palazzo, A., & Marsano, R. M. (2024) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2024.169942 · Cited by 14 · see citing works
Honeybee as a food nutrition analysis model of neural development and gut microbiota
Huang, Y., Li, N., Yang, C., Lin, Y., Wen, Y., Zheng, L., & Zhao, C. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105372 · Cited by 11 · see citing works
Foraging behaviour of medfly larvae is affected by maternally transmitted and environmental bacteria
Sivakala, K. K., Jose, P. A., Shamir, M., Wong, A. C.-N., Jurkevitch, É., & Yuval, B. (2021) · Animal Behaviour · doi:10.1016/j.anbehav.2021.10.014 · Cited by 10 · see citing works
A theoretical exploration of dietary collective medication in social insects
Poissonnier, L., Lihoreau, M., Gómez‐Moracho, T., Dussutour, A., & Buhl, C. (2017) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2017.08.005 · Cited by 10 · see citing works
Gato, W. E., Posick, C., Williams, A. A., & Mays, C. A. (2017) · Deviant Behavior · doi:10.1080/01639625.2017.1410373 · Cited by 10 · see citing works
Welfare Indicators for Aquaculture Research: Toolboxes for Five Farmed European Fish Species
Chris, N., Abbink, W., Alvestad, R., Ardó, L., Bégout, M., Bloecher, N., Burgerhout, E., Calduch-Giner, J. À., Chivite, M., Císař, P., et al. (2025) · Reviews in Aquaculture · doi:10.1111/raq.70109 · Cited by 12 · see citing works
Sieksmeyer, T., He, S., Esparza-Mora, M. A., Jiang, S., Petrašiūnaitė, V., Kuropka, B., Banasiak, R., Julseth, M. J., Weise, C., Johnston, P. R., et al. (2022) · BMC Ecology and Evolution · doi:10.1186/s12862-022-02007-8 · Cited by 9 · see citing works
Modelling the evolution of holobionts: an incomplete review
Rodrigo, A. G. (2023) · New Zealand Journal of Zoology · doi:10.1080/03014223.2023.2255142 · Cited by 9 · see citing works
Goswami, S., Das, S. B., Rath, P. C., Adak, T., Parameswaran, C., Jambhulkar, N. N., Govindharaj, G., Gadratagi, B. G., Patil, N. B., Mohapatra, S. D., et al. (2024) · Journal of Asia-Pacific Entomology · doi:10.1016/j.aspen.2024.102229 · Cited by 8 · see citing works
Frank, C. E., Sadeghi, J., Heath, D. D., & Semeniuk, C. A. D. (2024) · Genes Brain & Behavior · doi:10.1111/gbb.12898 · Cited by 6 · see citing works
Zebrafish ( Danio rerio ) behavioral phenotypes are not underscored by different gut microbiomes
Ayayee, P. A., & Wong, R. Y. (2024) · Ecology and Evolution · doi:10.1002/ece3.70237 · Cited by 6 · see citing works
The Effect of Non‐Self Genes on the Behaviour of Hosts
Wedell, N. (2019) · Wiley eBooks · doi:10.1002/9781119313663.ch8 · Cited by 4 · see citing works
Interkingdom Community Interactions in Disease Ecology
Benbow, M. E., Pechal, J. L., Tomberlin, J. K., & Jordan, H. R. (2018) · Advances in environmental microbiology · doi:10.1007/978-3-319-92373-4_1 · Cited by 3 · see citing works
Yuval, B., Lahuatte, P. F., Jose, P. A., Causton, C. E., Jurkevitch, É., Kouloussis, N. A., & Ben‐Yosef, M. (2019) · Insects · doi:10.3390/insects10120431 · Cited by 2 · see citing works
Myalgic encephalomyelitis / chronic fatigue syndrome as a breakdown of homeostasisPreprint
Marks, D. F. (2021) · Qeios · doi:10.32388/fz1y68.2 · Cited by 1 · see citing works
Zebrafish ( Danio rerio ) behavioral phenotypes not underscored by different gut microbiotaPreprint
Ayayee, P. A., & Wong, R. Y. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.05.29.596447 · Cited by 2 · see citing works
The microbiome and host behaviour
Lizé, A., & Lewis, Z. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108654418.006 · Cited by 1 · see citing works
Editorial overview: Hidden players: microbes reshape the insect niche
Trumbo, S. T., & Klassen, J. L. (2020) · Current Opinion in Insect Science · doi:10.1016/j.cois.2020.05.008 · Cited by 1 · see citing works
Myalgic encephalomyelitis / chronic fatigue syndrome as a breakdown of homeostasisPreprint
Marks, D. F. (2022) · Qeios · doi:10.32388/fz1y68.3 · Cited by 1 · see citing works
Goswami, S., Das, S., & Rath, P. C. (2023) · Research Biotica · doi:10.54083/resbio/5.3.2023/97-101
Human gut microbiota and regulation of human behavior
Noel, J. K., Mahadevan, M., Umesh, M., & Suresh, S. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-33351-4.00020-9
Eterovick, P. C., Glos, J., Burkart, F., Overmann, J., & Ruthsatz, K. (2026) · Environmental Microbiology · doi:10.1111/1462-2920.70331
Balardin, R. R., Nora, D. D., Rosado, Y. Z. F., Hardy, I. C. W., Godoy‐Vitorino, F., & Rodrigues, J. C. V. (2026) · Biological Control · doi:10.1016/j.biocontrol.2026.106100
Origins of termite eusociality: developmental foundations
Nalepa, C. A. (2026) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2026.1836415
Bollina, S., Zardi, G. I., Cuvillier‐Hot, V., Tilliette, C., Brigant, E., Holl, A.-C., & Nicastro, K. R. (2026) · Molecular Ecology · doi:10.1111/mec.70524
Ramniwas, S., Kumar, G., & Kalariya, D. (2026) · Ethology Ecology & Evolution · doi:10.1080/03949370.2026.2703127
- Authors
- Wong, A. C.-N., Holmes, A., Ponton, F., Lihoreau, M., Wilson, K., Raubenheimer, D., & Simpson, S. J.
- Affiliations
- Boston Children's Hospital (US)
- The University of Sydney (AU)
- Centre National de la Recherche Scientifique (FR)
- Lancaster University (GB)
- Corresponding author
- Wong, Adam C.-N.
- Holmes, Andrew
- ORCID
- Venue
- Frontiers in Microbiology
- Publisher
- Frontiers Media SA
- Published
- 2015-11-27
- Volume
- 6
- Pages
- 1359-1359
- ISSN
- 1664-302X (ISSN-L)
- PMC
- PMC4661234
- OpenAlex
- W2196244248
- Cited by
- 61
- References
- 97
- Citations by year
- 2026: 5 · 2025: 2 · 2024: 7 · 2023: 4 · 2022: 3 · 2021: 6 · 2020: 5 · 2019: 6 · 2018: 8 · 2017: 11 · 2016: 4
- FWCI
- 3.31
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Microbiology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- HAL (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Lancaster EPrints (Lancaster University) (submittedVersion)
- Funders
- Australian Research Council (DP130103222)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Physical Sciences › Environmental Science › Ecology › Parasite Biology and Host Interactions
- Keywords
- host-microbe interactions, holobiont, microbiome, animal behavior, host-parasite interactions, microbial interactions, host nutrition, nutritional geometry, nutrient intake
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