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Diet induces parallel changes to the gut microbiota and problem solving performance in a wild bird

  • 1.

    Cryan, J. F. & Dinan, T. G. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 13, 701–712 (2012).

    CAS  PubMed  Article  Google Scholar 

  • 2.

    Sherwin, E., Bordenstein, S. R., Quinn, J. L., Dinan, T. G. & Cryan, J. F. Microbiota and the social brain. Science (80-) 366, eaar2016 (2019).

    CAS  Article  Google Scholar 

  • 3.

    Heijtz, R. D. et al. Normal gut microbiota modulates brain development and behavior. Proc. Natl. Acad. Sci. 108, 3047–3052 (2011).

    ADS  CAS  Article  Google Scholar 

  • 4.

    Foster, J. A. & McVey Neufeld, K.-A. Gut–brain axis: how the microbiome influences anxiety and depression. Trends Neurosci. 36, 305–312 (2013).

    CAS  PubMed  Article  Google Scholar 

  • 5.

    Clarke, G. et al. The microbiome-gut–brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol. Psychiatry 18, 666–673 (2013).

    CAS  PubMed  Article  Google Scholar 

  • 6.

    Desbonnet, L., Clarke, G., Shanahan, F., Dinan, T. G. & Cryan, J. F. Microbiota is essential for social development in the mouse. Mol. Psychiatry 19, 146–148 (2014).

    CAS  PubMed  Article  Google Scholar 

  • 7.

    Hoban, A. E. et al. The microbiome regulates amygdala-dependent fear recall. Mol. Psychiatry 23, 1134–1144 (2018).

    CAS  PubMed  Article  Google Scholar 

  • 8.

    Magnusson, K. R. et al. Relationships between diet-related changes in the gut microbiome and cognitive flexibility. Neuroscience 300, 128–140 (2015).

    CAS  PubMed  Article  Google Scholar 

  • 9.

    Ogbonnaya, E. S. et al. Adult Hippocampal Neurogenesis Is Regulated by the Microbiome. Biol. Psychiat. 78, e7–e9 (2015).

    PubMed  Article  Google Scholar 

  • 10.

    Gareau, M. G. et al. Bacterial infection causes stress-induced memory dysfunction in mice. Gut 60, 307–317 (2011).

    PubMed  Article  Google Scholar 

  • 11.

    Stilling, R. M. et al. The neuropharmacology of butyrate: the bread and butter of the microbiota-gut–brain axis?. Neurochem. Int. 99, 110–132 (2016).

    CAS  PubMed  Article  Google Scholar 

  • 12.

    Davidson, G. L., Raulo, A. & Knowles, S. C. L. Identifying microbiome-mediated behaviour in wild vertebrates. Trends Ecol. Evol. https://doi.org/10.1016/j.tree.2020.06.014 (2020).

    Article  PubMed  Google Scholar 

  • 13.

    Davidson, G. L., Cooke, A. C., Johnson, C. N. & Quinn, J. L. The gut microbiome as a driver of individual variation in cognition and functional behaviour. Philos. Trans. R. Soc. B Biol. https://doi.org/10.1098/rstb.2017.0286 (2018).

    Article  Google Scholar 

  • 14.

    Morand-Ferron, J., Cole, E. F. & Quinn, J. L. Studying the evolutionary ecology of cognition in the wild: a review of practical and conceptual challenges. Biol. Rev. 91, 367–389 (2016).

    PubMed  Article  Google Scholar 

  • 15.

    Stephens, D. W. & Krebs, J. R. Foraging Theory (Princeton University Press, Princeton, 2019).https://doi.org/10.2307/j.ctvs32s6b

    Google Scholar 

  • 16.

    De Filippo, C. et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. U. S. A. 107, 14691–14696 (2010).

    ADS  PubMed  PubMed Central  Article  Google Scholar 

  • 17.

    Gillingham, M. A. F. et al. Offspring microbiomes differ across breeding sites in a panmictic species. Front. Microbiol. https://doi.org/10.3389/fmicb.2019.00035 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  • 18.

    Costa, S., Lopes, I., Proença, D. N., Ribeiro, R. & Morais, P. V. Diversity of cutaneous microbiome of Pelophylax perezi populations inhabiting different environments. Sci. Total Environ. 572, 995–1004 (2016).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 19.

    Knutie, S. A., Chaves, J. A. & Gotanda, K. M. Human activity can influence the gut microbiota of Darwin’s finches in the Galapagos Islands. Mol. Ecol. 28, 2441–2450 (2019).

    PubMed  Article  Google Scholar 

  • 20.

    Amato, K. R. et al. The gut microbiota appears to compensate for seasonal diet variation in the Wild Black Howler Monkey (Alouatta pigra). Microb. Ecol. 69, 434–443 (2014).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • 21.

    Hicks, A. L. et al. Gut microbiomes of wild great apes fluctuate seasonally in response to diet. Nat. Commun. 9, 1786 (2018).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 22.

    Maurice, C. F. et al. Marked seasonal variation in the wild mouse gut microbiota. ISME J. 9, 2423–2434 (2015).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 23.

    Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K. & Knight, R. Diversity, stability and resilience of the human gut microbiota. Nature 489, 220–230 (2012).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 24.

    Pan, D. & Yu, Z. Intestinal microbiome of poultry and its interaction with host and diet. Gut Microbes 5, 108–119 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  • 25.

    Teyssier, A. et al. Diet contributes to urban-induced alterations in gut microbiota: experimental evidence from a wild passerine. Proc. R. Soc. B Biol. Sci. https://doi.org/10.1098/rspb.2019.2182 (2020).

    Article  Google Scholar 

  • 26.

    David, L. A. et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559–563 (2014).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 27.

    Clarke, S. F. et al. Exercise and associated dietary extremes impact on gut microbial diversity. Gut 63, 1913–1920 (2014).

    CAS  PubMed  Article  Google Scholar 

  • 28.

    Fava, F. et al. The type and quantity of dietary fat and carbohydrate alter faecal microbiome and short-chain fatty acid excretion in a metabolic syndrome ‘at-risk’ population. Int. J. Obes. 37, 216–223 (2013).

    CAS  Article  Google Scholar 

  • 29.

    Wu, G. D. et al. Comparative metabolomics in vegans and omnivores reveal constraints on diet-dependent gut microbiota metabolite production. Gut 65, 63–72 (2016).

    CAS  PubMed  Article  Google Scholar 

  • 30.

    Zimmer, J. et al. A vegan or vegetarian diet substantially alters the human colonic faecal microbiota. Eur. J. Clin. Nutr. 66, 53–60 (2012).

    CAS  PubMed  Article  Google Scholar 

  • 31.

    Youngblut, N. D. et al. Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades. Nat. Commun. 10, 2200 (2019).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 32.

    Hird, S. M., Sánchez, C., Carstens, B. C. & Brumfield, R. T. Comparative gut microbiota of 59 neotropical bird species. Front. Microbiol. 6, 1403 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  • 33.

    Kartzinel, T. R., Hsing, J. C., Musili, P. M., Brown, B. R. P. & Pringle, R. M. Covariation of diet and gut microbiome in African megafauna. Proc. Natl. Acad. Sci. U. S. A. 116, 23588–23593 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 34.

    Bolnick, et al. The ecology of individuals: incidence and implications of individual specialization. Am. Nat. 161, 1–28 (2003).

    MathSciNet  PubMed  Article  Google Scholar 

  • 35.

    Li, W., Dowd, S. E., Scurlock, B., Acosta-Martinez, V. & Lyte, M. Memory and learning behavior in mice is temporally associated with diet-induced alterations in gut bacteria. Physiol. Behav. 96, 557–567 (2009).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 36.

    Ezra-Nevo, G., Henriques, S. F. & Ribeiro, C. The diet-microbiome tango: how nutrients lead the gut brain axis. Curr. Opin. Neurobiol. 62, 122–132 (2020).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 37.

    Psaltopoulou, T. et al. Mediterranean diet, stroke, cognitive impairment, and depression: a meta-analysis. Ann. Neurol. 74, 580–591 (2013).

    PubMed  Article  PubMed Central  Google Scholar 

  • 38.

    Carlson, A. L. et al. Infant gut microbiome associated with cognitive development. Biol. Psychiatry 83, 148–159 (2018).

    PubMed  Article  PubMed Central  Google Scholar 

  • 39.

    Dunn, J. C., Cole, E. F. & Quinn, J. L. Personality and parasites: Sex-dependent associations between avian malaria infection and multiple behavioural traits. Behav. Ecol. Sociobiol. 65, 1459–1471 (2011).

    Article  Google Scholar 

  • 40.

    Cole, E. F., Morand-Ferron, J., Hinks, A. E. & Quinn, J. L. Cognitive ability influences reproductive life history variation in the wild. Curr. Biol. 22, 1808–1812 (2012).

    CAS  PubMed  Article  Google Scholar 

  • 41.

    Seed, A. & Mayer, C. Problem Solving. in APA handbook of comparative psychology: Perception, learning, and cognition, Vol. 2 601–625 (American Psychological Association, 2017).

  • 42.

    Cole, E. F., Cram, D. L. & Quinn, J. L. Individual variation in spontaneous problem-solving performance among wild great tits. Anim. Behav. 81, 491–498 (2011).

    Article  Google Scholar 

  • 43.

    Morand-Ferron, J., Cole, E. F., Rawles, J. E. C. & Quinn, J. L. Who are the innovators? A field experiment with 2 passerine species. Behav. Ecol. 22, 1241–1248 (2011).

    Article  Google Scholar 

  • 44.

    Quinn, J. L., Cole, E. F., Reed, T. E. & Morand-Ferron, J. Environmental and genetic determinants of innovativeness in a natural population of birds. Philos. Trans. R. Soc. Biol. B Sci. 371, 20150184 (2016).

    Article  CAS  Google Scholar 

  • 45.

    Ducatez, S., Clavel, J. & Lefebvre, L. Ecological generalism and behavioural innovation in birds: technical intelligence or the simple incorporation of new foods?. J. Anim. Ecol. 84, 79–89 (2015).

    PubMed  Article  Google Scholar 

  • 46.

    Reader, S. M. & MacDonald, K. Environmental variability and primate behavioural flexibility. Anim. Innov. https://doi.org/10.1093/acprof:oso/9780198526223.003.0004 (2012).

    Article  Google Scholar 

  • 47.

    Biard, C. et al. Growing in cities: an urban penalty for wild birds? A study of phenotypic differences between urban and rural great tit chicks (Parus major). Front. Ecol. Evol. https://doi.org/10.3389/fevo.2017.00079 (2017).

    Article  Google Scholar 

  • 48.

    Teyssier, A. et al. Inside the guts of the city: urban-induced alterations of the gut microbiota in a wild passerine. Sci. Total Environ. 612, 1276–1286 (2018).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 49.

    Escallón, C., Belden, L. K. & Moore, I. T. The cloacal microbiome changes with the breeding season in a wild bird. Integr. Org. Biol. https://doi.org/10.1093/iob/oby009 (2019).

    Article  Google Scholar 

  • 50.

    Waite, D. W. & Taylor, M. W. Characterizing the avian gut microbiota: membership, driving influences, and potential function. Front. Microbiol. https://doi.org/10.3389/fmicb.2014.00223 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  • 51.

    Singh, R. K. et al. Influence of diet on the gut microbiome and implications for human health. J. Transl. Med. 15, 73 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 52.

    Knutie, S. A. Food supplementation affects gut microbiota and immunological resistance to parasites in a wild bird species. J. Appl. Ecol. 57, 536–547 (2020).

    CAS  Article  Google Scholar 

  • 53.

    Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 54.

    Veľký, M., Kaňuch, P. & Krištín, A. Food composition of wintering great tits (Parus major): habitat and seasonal aspects. Folia Zool. 60, 228–236 (2011).

    Article  Google Scholar 

  • 55.

    Phillips, J. N., Berlow, M. & Derryberry, E. P. The effects of landscape urbanization on the gut microbiome: an exploration into the gut of urban and rural white-crowned Sparrows. Front. Ecol. Evol. 6, 148 (2018).

    Article  Google Scholar 

  • 56.

    Rosshart, S. P. et al. Wild mouse gut microbiota promotes host fitness and improves disease resistance. Cell 171, 1015–1028 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 57.

    Griffin, A. S. & Guez, D. Innovation and problem solving: a review of common mechanisms. Behav. Process. 109, 121–134 (2014).

    Article  Google Scholar 

  • 58.

    Alcock, J., Maley, C. C. & Aktipis, C. A. Is eating behavior manipulated by the gastrointestinal microbiota? Evolutionary pressures and potential mechanisms. BioEssays 36, 940–949 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  • 59.

    Maniscalco, J. W. & Rinaman, L. Vagal interoceptive modulation of motivated behavior. Physiology 33, 151–167 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 60.

    Bruce-Keller, A. J. et al. Obese-type gut microbiota induce neurobehavioral changes in the absence of obesity. Biol. Psychiatry 77, 607–615 (2015).

    PubMed  Article  PubMed Central  Google Scholar 

  • 61.

    Greyson-Gaito, C. J. et al. Into the wild: microbiome transplant studies need broader ecological reality. Proc. R. Soc. B Biol. Sci. https://doi.org/10.1098/rspb.2019.2834 (2020).

    Article  Google Scholar 

  • 62.

    Roager, H. M. & Dragsted, L. O. Diet-derived microbial metabolites in health and disease. Nutr. Bull. 44, 216–227 (2019).

    Article  Google Scholar 

  • 63.

    Möhle, L. et al. Ly6Chi monocytes provide a link between antibiotic-induced changes in gut microbiota and adult hippocampal neurogenesis. Cell Rep. 15, 1945–1956 (2016).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • 64.

    Cryan, J. F. et al. The microbiota-gut-dbrain axis. Physiol. Rev. 99, 1877–2013 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 65.

    Heintz-Buschart, A. & Wilmes, P. Human gut microbiome: function matters. Trends Microbiol. 26, 563–574 (2018).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 66.

    O’Connor, R. J. Identification guide to European Passerines L. Svensson. Auk 102, (1985).

  • 67.

    Khan, G., Kangro, H. O., Coates, P. J. & Heath, R. B. Inhibitory effects of urine on the polymerase chain reaction for cytomegalovirus DNA. J. Clin. Pathol. 44, 360–365 (1991).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 68.

    Eisenhofer, R. et al. Contamination in low microbial biomass microbiome studies: issues and recommendations. Trends Microbiol. 27, 105–117 (2019).

    CAS  PubMed  Article  Google Scholar 

  • 69.

    Perrins, C. M. Tits and their caterpillar food supply. Ibis (Lond. 1859) 133, 49–54 (1991).

    Article  Google Scholar 

  • 70.

    Serrano-Davies, E., O’Shea, W. & Quinn, J. L. Individual foraging preferences are linked to innovativeness and personality in the great tit. Behav. Ecol. Sociobiol. 71, 161 (2017).

    Article  Google Scholar 

  • 71.

    Aplin, L. M., Sheldon, B. C. & McElreath, R. Conformity does not perpetuate suboptimal traditions in a wild population of songbirds. Proc. Natl. Acad. Sci. U. S. A. 114, 7830–7837 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 72.

    O’Shea, W., Serrano-Davies, E. & Quinn, J. L. Do personality and innovativeness influence competitive ability? An experimental test in the great tit. Behav. Ecol. 28, 1435–1444 (2017).

    Article  Google Scholar 

  • 73.

    Shutt, J. D. et al. Gradients in richness and turnover of a forest passerine’s diet prior to breeding: a mixed model approach applied to faecal metabarcoding data. Mol. Ecol. 29, 1199–1213 (2020).

    PubMed  Article  Google Scholar 

  • 74.

    Crouch, N. M. A., Lynch, V. M. & Clarke, J. A. A re-evaluation of the chemical composition of avian urinary excreta. J. Ornithol. 161, 17–24 (2020).

    Article  Google Scholar 

  • 75.

    Fouhy, F. et al. Perinatal factors affect the gut microbiota up to four years after birth. Nat. Commun. 10, 1517 (2019).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 76.

    Konstantinidis, K. T. & Tiedje, J. M. Genomic insights that advance the species definition for prokaryotes. Proc. Natl. Acad. Sci. U. S. A. 102, 2567–2572 (2005).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 77.

    McMurdie, P. J. & Holmes, S. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217 (2013).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 78.

    R Core Team. R: A language and environment for statistical computing. R Found. Stat. Comput. Vienna, Austria. https://www.R-project.org/ (2014).

  • 79.

    Bokulich, N. A. et al. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat. Methods 10, 57–59 (2013).

    CAS  PubMed  Article  Google Scholar 

  • 80.

    Di Rienzi, S. C. et al. The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to Cyanobacteria. Elife https://doi.org/10.7554/eLife.01102 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  • 81.

    Bates, D., Maechler, M., Bolker, B. & Walker, S. lme4: linear mixed-effects models using Eigen and S4. R package version 1.1–7, https://CRAN.R-project.org/package=lme4. R Packag. version (2014).

  • 82.

    Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest package: tests in linear mixed effects models. J. Stat. Softw. https://doi.org/10.18637/jss.v082.i13 (2017).

    Article  Google Scholar 

  • 83.

    Zakrzewski, M. et al. Calypso: a user-friendly web-server for mining and visualizing microbiome-environment interactions. Bioinformatics https://doi.org/10.1093/bioinformatics/btw725 (2017).

    Article  PubMed  Google Scholar 


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