Jump to ContentJump to Main Navigation
Show Summary Details

Co-evolution in context: The importance of studying gut microbiomes in wild animals

Katherine R. Amato
  • Program in Ecology Evolution and Conservation Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA, 61801
  • Department of Anthropology, University of Illinois at Urbana-Champaign, Urbana, IL, USA, 61801
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2013-10-22 | DOI: https://doi.org/10.2478/micsm-2013-0002

Abstract

Because the gut microbiota contributes to host nutrition, health and behavior, and gut microbial community composition differs according to host phylogeny, co-evolution is believed to have been an important mechanism in the formation of the host-gut microbe relationship. However, current research is not ideal for examining this theme. Most studies of the gut microbiota are performed in controlled settings, but gut microbial community composition is strongly influenced by environmental factors. To truly explore the co-evolution of host and microbe, it is necessary to have data describing host-microbe dynamics in natural environments with variation in factors such as climate, food availability, disease prevalence, and host behavior. In this review, I use current knowledge of host-gut microbe dynamics to explore the potential interactions between host and microbe in natural habitats. These interactions include the influence of host habitat on gut microbial community composition as well as the impacts of the gut microbiota on host fitness in a given habitat. Based on what we currently know, the potential connections between host habitat, the gut microbiota, and host fitness are great. Studies of wild animals will be an essential next step to test these connections and to advance our understanding of host-gut microbe co-evolution.

Keywords: Gut microbiota; host-microbe; co-evolution; habitat; ecology; fitness

  • [1] Forsythe P., Sudo N., Dinan T., Taylor V.H., Bienenstock J. Mood and gut feelings. Brain Behav Immun 2010; 24: 9-16 Google Scholar

  • [2] Flint H.J., Bayer E.A. Plant cell wall breakdown by anaerobic microorganisms from the mammalian digestive tract. Ann NY Acad Sci 2008: 280-288 Google Scholar

  • [3] Flint H.J., Duncan S.H., Louis P., Impact of intestinal microbial communities upon health., In: Rosenberg E, Gophna U. (Eds.), Beneficial Microorganisms in Multicellular Life Forms Springer, Berlin, 2011 243-252. Google Scholar

  • [4] Sekirov I., Russel S.I., Antunes C.M., Finlay B.B. Gut microbiota in health and disease. Physiol Rev 2010; 90: 859- 904 Google Scholar

  • [5] Hooper L.V., Littman D.R., Macpherson A.J. Interactions between the microbiota and the immune system. Science 2012; 336: 1268-1273 Google Scholar

  • [6] Hooper L.V., Midtvedt T., Gordon J.I. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 2002; 22: 283-307 Google Scholar

  • [7] Dethlefsen L., McFall-Ngai M., Relman D.A. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 2007; 449: 811-818 Google Scholar

  • [8] Sudo N. Stress and gut microbiota: does postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response? Int Cong Ser 2006; 1287: 350-354 Google Scholar

  • [9] Sudo N., Chida Y., Aiba Y., Sonoda J., Oyama N., Yu X.N., et al. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol 2004; 558: 263-275 Google Scholar

  • [10] Sharon G., Segal D., Ringo J.M., Hefetz A., Zilber-Rosenberg I., Rosenberg E. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci USA 2010; 107: 20051 Google Scholar

  • [11] Hill M.J. Intestinal flora and endogenous vitamin synthesis. Eur J Cancer Prev 1997; 6: S43-S45 Google Scholar

  • [12] Neish A.S. Microbes in gastrointestinal health and disease. Gastroenterol 2009; 136: 65-80 Google Scholar

  • [13] Brinkworth G.D., Noakes M., Clifton P.M., Bird A.R. Comparative effects of very low-carbohydrate, high-fat and high-carbohydrate, low-fat weight-loss diets on bowel habit and faecal short-chain fatty acids on bacterial populations. Br J Nutr 2009; 101: 1493-1502 Google Scholar

  • [14] Donohoe D.R., Garge N., Zhang X., Sun W., O’Connell T.M., Bunger M.K., et al. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab 2011; 13: 517-526 Google Scholar

  • [15] Duncan S.H., Belenguer A., Holtrop G., Johnstone A.M., Flint H.J., Lobley G.E. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of buyrate and butyrate-producing bacteria in feces. Appl Environ Microbiol 2007; 73: 1073-1078 Google Scholar

  • [16] Duncan S.H., Scott K.P., Ramsay A.G., al. e. Effects of alternative dietary substrates on competition between human colonic bacteria in an anaerobic fermentor system. Appl Environ Microbiol 2003; 69: 1136-1142 Google Scholar

  • [17] Macfarlane G.T., Cummings J.H., Allison C. Protein degradation by human intestinal bacteria. Microbiology 1986; 132: 1647-1656 Google Scholar

  • [18] Macfarlane S., Macfarlane G.T. Regulation of short-chain fatty acid production. Proc Nutr Soc 2003; 65: 67-72 Google Scholar

  • [19] Fraser M.D., Theobald V.J., Davies D.R., Moorby J.M. Impact of diet selected by cattle and sheep grazing heathland communities on nutrient supply and faecal micro-flora activity. Agric Ecosyst Environ 2009; 129: 367-377 Google Scholar

  • [20] Flint H.J., Scott K.P., Duncan S.H., Louis P., Forano E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes 2012; 3: 289-306 Google Scholar

  • [21] Nicholson J.K., Holmes E., Kinross J., Burcelin R., Gibson G., Jia W., et al. Host-gut microbiota metabolic interactions. Science 2012; 336: 1262-1267 Google Scholar

  • [22] Secor S.M. Regulation of digestive performance: a proposed adaptive response. Comp Biochem Physiol 2001; 128: 565- 577 Google Scholar

  • [23] Turnbaugh P.J., Ley R.E., Mahowald M.A., Magrini V., Mardis E.R., Gordon J.I. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006; 444: 1027-1031 Google Scholar

  • [24] Mackie R.I., Sghir A., Gaskins H.R. Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr 1999; 69: 1035S-1045S Google Scholar

  • [25] Turnbaugh P.J., Ridaura V.K., Faith J.J., Rey F.E., Knight R., Gordon H.A. The effect of diet on the human gut microbiome: A metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 2009; 1: 6ra14 Google Scholar

  • [26] Muegge B.D., Kuczynski J., Knights D., Clemente J.C., Gonzalez A., Fontana L., et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 2011; 332: 970-974 Google Scholar

  • [27] Wu G.D., Chen J., Hoffmann C., Bittinger K., Chen Y.Y., Keilbaugh S.A., et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011; 334: 105-108 Google Scholar

  • [28] Benson A.K., Kelly S.A., Legge R., Ma F., Low S.J., Kim J., et al. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors Proc Natl Acad Sci USA 2010; 107: 18933- 18938 Google Scholar

  • [29] Arumugam M., Raes J., Pelletier E., Le Paslier D., Yamada T., Mende D.R., et al. Enterotypes of the human gut microbiome. Nature 2011; 473: 174-180 Google Scholar

  • [30] Costello E.K., Stagaman K., Dethlefsen L., Bohannan B.J., Relman D.A. An application of ecological theory toward an understanding of the human microbiome. Science 2012; 336: 1255-1262 Google Scholar

  • [31] Friswell M.K., Gika H., Stratford I.J., Theodoridis G., Telfer B., Wilson I.D., et al. Site and strain-specific variation in gut microbiota profiles and metabolism in experimental mice. PLoS One 2010; 5: e8584 Google Scholar

  • [32] Buhnik-Rosenblau K., Danin-Poleg Y., Kashi Y., Host genetics and gut microbiota., In: Rosenberg E, Gophna U. (Eds.), Beneficial Microorganisms in Multicellular Life Forms Springer, Berlin, 2011 281-295. Google Scholar

  • [33] Zoetendal E.G., Akkermans A.D.L., Akkermans-va Vliet W.M., de Visser J.A.G.M., De Vos W.M. The host genotype affects the bacterial community in the human gastrointestinal tract. Microb Ecol Health Dis 2001; 13: 129-134 Google Scholar

  • [34] Ley R.E., Hamady M., Lozupone C., Turnbaugh P.J., Ramey R.R., Bircher J.S., et al. Evolution of mammals and their gut microbes. Science 2008; 320: 1647-1651 Google Scholar

  • [35] Ley R.E., Lozupone C., Hamady M., Knight R., Gordon H.A. Worlds within worlds: Evolution of the vertebrate gut microbiota. Nature 2008; 6: 776-788 Google Scholar

  • [36] Yeoman C.J., Chia N., Yildirim S., Berg Miller M.E., Kent A., Stumpf R.M., et al. Towards an evolutionary model of animalassociated microbiomes. Entropy 2011; 13: 570-594 Google Scholar

  • [37] Kau A.L., Abern P.P., Griffin N.W., Goodman A.L., Gordon J.I. Human nutrition, the gut microbiome and the immune system. Nature 2011; 474: 327-336 Google Scholar

  • [38] Savage D.C. Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 1977; 31: 107-133 Google Scholar

  • [39] Schramm A., Davidson S.K., Dodsworth J.A., Drake H.L., Stahl D.A., Dubilier N. Acidovorax-like symbionts in the nephridia of earthworms. Environ Microbiol 2003; 5: 804-809 Google Scholar

  • [40] McFall-Ngai M. Adaptive immunity: Care for the community. Nature 2007; 445: 153 Google Scholar

  • [41] Backhed F., Manchester J.K., Semenkovich C.F., Gordon J.I. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci USA 2007; 104: 979-984 Google Scholar

  • [42] Bauer H., Horowitz R.E., Levenson S.M., Popper H. The response of the lymphatic tissue to the microbial flora. Studies on germfree mice. Am J Pathol 1963; 42: 471-483 PubMedGoogle Scholar

  • [43] Faith J.J., McNulty N.P., Rey F.E., Gordon J.I. Predicting a human gut microbiota’s response to diet in gnotobiotic mice. Science 2011; 333: 101-104 Google Scholar

  • [44] Armougom F., Henry M., Vialettes B., Raccah D., Raoult D. Monitoring bacterial community of human gut microbiota reveals an increase in Lactobacillus in obese patients and Methanogens in aneroxic patients. PLoS One 2009; 4: e7125 Google Scholar

  • [45] Costello E.K., Lauber C.L., Hamady M., Fierer N., Gordon J.I., Knight R. Bacterial community variation in human body habitats across space and time. Science 2009; 326: 1694- 1697 Google Scholar

  • [46] Kurokawa K., Itoh T., Kuwahara T., Oshima K., Toh H., Toyoda A., et al. Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Research 2007; 14: 169-181 Google Scholar

  • [47] Larsen N., Vogensen F.K., van den Berg F.W.J., Nielsen D.S., Andreasen A.S., Pedersen B.K., et al. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One 2010; 5: e9085 Google Scholar

  • [48] Ley R.E. Obesity and the human microbiome. Curr Opin Gastroenterol 2010; 26: 5-11 Google Scholar

  • [49] Mariat D., Firmesse O., Levenez F., Guimaraes V.D., Sokol H., Dore J., et al. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol 2009; 9: 123-129 Google Scholar

  • [50] Roeselers G., Mittge E.K., Stephens W.Z., Parichy D.M., Cavanaugh C.M., Guillemin K., et al. Evidence for a core gut microbiota in the zebrafish. ISME J 2011; 5: 1595-1608 Google Scholar

  • [51] Xenoulis P.G., Gray P.L., Brightsmith D., Palculict B., Hoppes S., Steinger J.M., et al. Molecular characterization of the cloacal microbiota of wild and captive parrots. Vet Microbiol 2010; 146: 320-325 Google Scholar

  • [52] Nelson T.M., Rogers T.L., Carlini A.R., Brown M.V. Diet and phylogeny shape the gut microbiota of Antarctic seals: A comparison of wild and captive animals. Environ Microbiol 2012; 15: 1132-1145 Google Scholar

  • [53] Amato K.R., Yeoman C.J., Kent A., Carbonero F., Righini N., Estrada A.E., et al. Habitat degradation impacts primate gastrointestinal microbiomes. 2013; 7: 1344-1353 Google Scholar

  • [54] Nakamura N., Amato K.R., Garber P.A., Estrada A.E., Mackie R.I., Gaskins H.R. Analysis of the hydrogenotrophic microbiota of wild and captive black howler monkeys (Alouatta pigra) in Palenque National Park, Mexico. Am J Primatol 2011; 73: 909-919 Google Scholar

  • [55] Schwab C., Cristescu B., Boyce M.S., Stenhouse G.B., Ganzle M. Bacterial populations and metabolites in the feces of free roaming and captive grizzly bears. Can J Microbiol 2009; 55: 1335-1346 PubMedGoogle Scholar

  • [56] Zhu L., Wu Q., Dai J., Zhang S., Fuwen W. Evidence of cellulose metabolism by the giant panda gut microbiome. Proc Natl Acad Sci USA 2011; 108: 17714-17719 Google Scholar

  • [57] Uenishi G., Fujita S., Ohashi G., Kato A., Yamauchi S., Matsuzawa T., et al. Molecular analyses of the intestinal microbiota of chimpanzees in the wild and in captivity. Am J Primatol 2007: 367-376 Google Scholar

  • [58] Dhanasiri A.K.S., Brunvold L., Brinchmann M.F., Korsnes K., Bergh O., Kiron V. Changes in the intestinal microbiota of wild Atlantic cod Gadus morhua L. upon captive rearing. Microbial Ecology 2011; 61: 20-30 Google Scholar

  • [59] Donnet-Hughes A., Perez P.F., Dore J., Leclerc M., Levenez F., Benyacoub J., et al. Potential role of the intestinal microbiota of the mother in neonatal immune education. Proc Nutr Soc 2010; 69: 407-415 Google Scholar

  • [60] Mshvildadze M., Neu J., Shuster J., Theriaque D., Li N., Mai V. Intestinal microbial ecology in premature infants assessed using non-culture based techniques. J Pediatr 2010; 156: 20-25 Google Scholar

  • [61] Jimenez E., Marin M.L., Martin R., Odriozola J.M., Olivares M., Xaus J., et al. Is meconium from healthy newborns actually sterile? Res Microbiol 2008; 159: 187-193 Google Scholar

  • [62] Hubbell S.P., The Unified Neutral Theory of Biodiversity and Biogeography. Princeton University Press, Princeton, New Jersey, 2001: Google Scholar

  • [63] Freeland W.J. Primate social groups as biological islands. Ecology 1979; 60: 719-728 Google Scholar

  • [64] Lankau E.W., Hong P.Y., Mackie R.I. Ecological drift and local exposures drive enteric bacterial community differences within species of Galapagos iguanas. Mol Ecol 2012; 21: 1779-1788 Google Scholar

  • [65] Fallani M., Young D., Scott J., Norin, E., Amarri S., Adam, R., et al. Intestinal microbiota of 6-week-old infants across Europe: Geographic influence beyond delivery mode, breastfeeding and antibiotics. J Pediatr Gastr Nutr 2010; 51: 77-84 Google Scholar

  • [66] Degnan P.H., Pusey A.E., Lonsdorf E.V., Goodall J., Wroblewski E.E., Wilson M.L., et al. Factors associated with the diversification of the gut microbial communities within chimpanzees from Gombe National Park. Proc Natl Acad Sci USA 2012; 109: 13034-13039 Google Scholar

  • [67] Pavelka M.S., Mechanisms of cohesion in black howler monkeys., In: Susmann RW, Cloninger CR, editors, Origins of altruism and cooperation Springer, New York, 2011 167- 178. Google Scholar

  • [68] Chapman C.A., Chapman L.J., Wrangham R.W. Ecological constraints on group size - An analysis of spider monkey and chimpanzee subgroups. Behav Ecol Sociobiol 1995; 36: 59- 70 Google Scholar

  • [69] Bates L.A., Byrne R.W. Sex differences in the movement patterns of free-ranging chimpanzees (Pan troglodytes schweinfurthii): Foraging and border checking. Behav Ecol Sociobiol 2009; 64: 247-255 Google Scholar

  • [70] Sommer V., Mendoza-Granados D. Play as an indicator of habitat quality: A field study of Langur monkeys (Presbytis entellus). Ethology 1995; 99: 177-192 Google Scholar

  • [71] Barrett L., Dunbar R.I.M., Dunbar P. Environmental influences on play behaviour in immature gelada baboons. Anim Behav 1992; 44: 11-115 Google Scholar

  • [72] Banks S.C., Piggott M.P., Stow A.J., Taylor A.C. Sex and sociality in a disconnected world: A review of the impacts of habitat fragmentation on animal social interactions. Can J Zool 2007; 85: 1065-1079 Google Scholar

  • [73] Hart B.L., Hart L.A., Mooring M.S., Olubayo R. Biological basis of grooming behavior in antelope: The body-size, vigilance and habitat principles. Anim Behav 1992; 44: 615- 631 Google Scholar

  • [74] Hill R.A. Thermal constraints on activity scheduling and habitat choice in baboons. Am J Phys Anthr 2006; 129: 242- 249 Google Scholar

  • [75] Bowers M.A., Matter S.F. Landscape ecology of mammals: Relationships between density and patch size. J Mammal 1997; 78: 999-1013 Google Scholar

  • [76] Cristobal-Azkarate J., Arroyo-Rodriguez V. Diet and activity pattern of howler monkeys (Alouatta palliata) in Los Tuxtlas, Mexico: Effects of habitat fragmentation and implications for conservation. Am J Primatol 2007; 69: 1013-1029 Google Scholar

  • [77] Glessner K.D.G., Britt A. Population density and home range size of Indri indri in a protected low altitude rain forest. Int J Primatol 2005; 26: 855-872 Google Scholar

  • [78] Chiarello A.G., Melo F.R. Primate population densities and sizes in Atlantic forest remnants of northern Espirito Santo, Brazil. Int J Primatol 2001; 22: 379-396 Google Scholar

  • [79] Fahrig L. Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 2003; 34: 487-515 Google Scholar

  • [80] Altizer S., Nunn C.L., Thrall P.H., Gittleman J.L., Antonovis J., Cunningham A.A., et al. Social organization and parasite risk in mammals: integrating theory and empirical studies. Annu Rev Ecol Evol Syst 2003: 517-547 Google Scholar

  • [81] Johnson M.B., Lafferty K.D., van Oosterhout C., Cable J. Parasite transmission in social interacting hosts: Monogenean epidemics in guppies. PLoS One 2011; 6: e22634 Google Scholar

  • [82] Ryder J.J., Miller M.R., White A., Knell R.J., Boots M. Hostparasite population dynamics under combined frequencyand density-dependent transmission. Oikos 2007; 116: 2017-2026 Google Scholar

  • [83] Arneberg P., Skorping A., Grenfell B., Read A.F. Host densities as determinants of abundance in parasite communities. Proc Royal Soc B 1998; 265: 1283-1289 Google Scholar

  • [84] McNulty N.P., Yatsunenko T., Hsaio A., Faith J.J., Muegge B.D., Goodman A.L., et al. The impact of a consortium of fermented milk strains on the gut microbiome of gnotobiotic mice and monozygotic twins. Sci Transl Med 2011; 3: 1-14 Google Scholar

  • [85] Fons M., Gomez A., Karjalainen T. Mechanisms of colonisation resistance of the digestive tract. Part 2: Bacteria/ bacteria interactions. Microb Ecol Health Dis 2000; 12: 240- 246 Google Scholar

  • [86] Servin A.L. Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol Rev 2004; 28: 405-440 Google Scholar

  • [87] Kennedy M.J., Volz P.A. Ecology of Candida albicans gut colonization: Inhibition of Candida adhesion, colonization, and dissemination from the gastrointestinal tract by bacterial antagonism. Infect Immun 1985; 49: 654-663 Google Scholar

  • [88] Turnbaugh P.J., Gordon H.A. The core gut microbiome, energy balance and obesity. J Physiol 2009; 587: 4153-4158 Google Scholar

  • [89] Turnbaugh P.J., Hamady M., Yatsunenko T., Cantarel B.L., Duncan A., Ley R.E., et al. A core gut microbiome in obese and lean twins. Nature 2009; 457: 480-484 Google Scholar

  • [90] Turnbaugh P.J., Ley R.E., Hamady M., Fraser-Liggett C.M., Knight R., Gordon J.I. The Human Microbiome Project. Nature 2007; 449: 804-810 Google Scholar

  • [91] Hamady M., Knight R. Microbial community profiling for human microbiome projects: Tools, techniques and challenges. Genome Res 2009; 19: 1141-1152 Google Scholar

  • [92] Shade A., Handelsman J. Beyond the Venn diagram: The hunt for a core microbiome. Environ Microbiol 2011; 14: 4-12 Google Scholar

  • [93] Degnan B.A., Transport and metabolism of carbohydrates by anaerobic gut bacteria. University of Cambridge, 1992 Google Scholar

  • [94] Flint H.J., Bayer E.A., Rincon M.T., Lamed R., White B.A. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nature 2008; 6: 121-131 Google Scholar

  • [95] Kohl K.D., Dearing M.D. Experience matters: Prior exposure to plant toxins enhances diversity of gut microbes in herbivores. Ecol Lett 2012; 15: 1008-1015 Google Scholar

  • [96] Cha H.R., Chang S.Y., Chang J.H., Kim J.O., Yang J.Y., Kim C.H., et al. Downregulation of Th17 cells in the small intestine by disruption of gut flora in the absence of retinoic acid. J Immunol 2010; 184: 6799-6806 Google Scholar

  • [97] Broderick N.A., Raffa K.F., Goodman R.M., Handelsman J. Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Appl Environ Microbiol 2004; 70: 293-300 Google Scholar

  • [98] Ringo E., Sperstad S., Myklebust R., Refstie S., Krogdahl A. Characterisation of the microbiota associated with intestine of Atlantic cod (Gadus morhua L.): The effect of fish meal, standard soybean meal and a bioprocessed soybean meal. Aquaculture 2006; 261: 829-841 Google Scholar

  • [99] Hildebrandt M.A., Hoffman C., Sherrill-Mix S.A., Keilbaugh S.A., Hamady M., Chen Y.Y., et al. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterol 2009; 137: 1716-1724 Google Scholar

  • [100] Williams C.L., Willard S., Kouba A., Sparks D., Holmes W., Falcone J., et al. Dietary shifts affect the gastrointestinal microflora of the giant panda (Ailuropoda melanoleuca). J Anim Physiol Anim Nutr 2012: Google Scholar

  • [101] Wang Y., Gilbreath T.M., III, Kukutla P., Yan G., Xu J. Dynamic gut microbiome across life history of the malaria mosquito Anopheles gambiae in Kenya. PLoS One 2011; 6: e24767 Google Scholar

  • [102] Cardoso A.M., Cavalcante J.V., Vieira R.P., Lima J.L., Grieco M.A.B., Clementino M.M., et al. Gut bacterial communities in the giant land snail Achatina fulica and their modification by sugarcane-based diet. PLoS One 2012; 7: e33440 Google Scholar

  • [103] Kane M.D., Breznak J.A. Effect of host diet on production of organic acids and methane by cockroach gut bacteria. Appl Environ Microbiol 1991; 57: 2628-2634 Google Scholar

  • [104] De Filippo C., Cavalieri D., Di Paola M., Ramazzotti M., Poullet J.B., Massart S., 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 USA 2010; 107: 14691-14696 Google Scholar

  • [105] Yatsunenko T., Rey F.E., Manary M.J., Trehan I., Dominguez- Bello M.G., Contreras M., et al. Human gut microbiome viewed across age and geography. Nature 2012: Google Scholar

  • [106] Marshall A.J., Boyko C.M., Feilen K.L., Boyko R.H., Leighton M. Defining fallback foods and assessing their importance in primate ecology and evolution. Am J Phys Anthr 2009; 140: 603-614 Google Scholar

  • [107] Hoffman R.R. Evolutionary steps of ecophysiological adaptation and diversification of ruminants: A comparative view of their digestive system. Oecologia 1989; 78: 443-457 Google Scholar

  • [108] Darwin C., On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. John Murray, London, 1859 Google Scholar

  • [109] Santos J.C., Coloma L.A., Cannatella D.C. Multiple recurring origins of aposematism and diet specialization in poison frogs. Pro Natl Acad Sci USA 2003; 100: 12792-12797 Google Scholar

  • [110] Lambert J.E., Primate nutritional ecology: Feeding biology and diet at ecological and evolutionary scales, In: Campbell C, Fuentes A, MacKinnon KC, Panger M, Bearder SK, (Eds.), Primates in Perspective, Second edition ed Oxford University Press, New York, 2011: 512-522. Google Scholar

  • [111] Leonard W.R., Robertson M.L. Evolutionary perspectives on human nutrition: The influence of brain and body-size on diet and metabolism. Am J Hum Biol 1994; 6: 77-88 Google Scholar

  • [112] Norconk M.A., Wright B.W., Conklin-Brittain N.L., Vinyard C.J., Mechanical and nutritional properties of food as factors in platyrrhine dietary adaptations, In: Garber PA, Bicca- Marques JC, Estrada AE, Heymann EW, Strier KB. (Eds.), South American Primates, Developments in Primatology: Progress and Prospects Springer, New York, 2009: 279-319. Google Scholar

  • [113] Ragir S. Diet and food preparation: Rethinking early hominid behavior. Evol Anthr 2000; 9: 153-155 Google Scholar

  • [114] Kaplan H., Hill K., Lancaster J., Hurtado A.M. A theory of human life history evolution: Diet, intelligence, and longevity. Evol Anthr 2000; 9: 156-185 Google Scholar

  • [115] Cordain L., Eaton S.B., Sebastian A., Mann N., Lindeberg S., Watkins B.A., et al. Origins and evolution of the Western diet: Health implications for the 21st century. Am J Clin Nutr 2005; 81: 341-354 Google Scholar

  • [116] Fleagle J.G., Primate Adaptation and Evolution. Academic Press, San Diego, 2013: Google Scholar

  • [117] Vrieze A., Holleman F., Zoetendal E.G., de Vos W.M., Hoekstra J.B.L., Nieuwdorp M. The environment within: how gut microbiota may influence metabolism and body composition. Diabetol 2010; 53: 606-613 Google Scholar

  • [118] Chivers D.J., Hladik C.M. Morphology of the gastrointestinal tract in primates: Comparisons with other mammals in relation to diet. J Morphol 1980; 166: 337-386 Google Scholar

  • [119] Milton K., The foraging strategy of howler monkeys. Columbia University Press, New York, 1980 Google Scholar

  • [120] Chapman C.A., Chapman L.J., Rode K.D., Hauck E.M., McDowell L.R. Variation in the nutritional value of primate foods: Among trees, time periods, and areas. Int J Primatol 2003; 24: 317-333 Google Scholar

  • [121] Gates J. Habitat alteration, hunting and the conservation of folivorous primates in African forests. Aust J Ecol 2006; 21: 1-9 Google Scholar

  • [122] Gonzalez V., Zunino G.E., Kowalewski M.M., Bravo S.P. Densidad de monos aulladores (Alouatta caraya) y composición y estructura de la selva de inundación en una isla del Río Paraná medio. Revista Mus Argentino de Ciencias Naturales 2002; 4: 7-12 Google Scholar

  • [123] Boinski S. Sex-differences in the foraging behavior of squirrel monkeys in a seasonal habitat. Behav Ecol Sociobiol 1988; 23: 177-186 Google Scholar

  • [124] van Schaik C.P., Terborgh J.W., Wright S.J. The phenology of tropical forests: Adaptive significance and consequences for primary consumers. Annu Rev Ecol Syst 1993; 24: 353-377 Google Scholar

  • [125] Albon S.D., Langvatn R. Plant phenology and the benefits of migration in a temperate ungulate. Oikos 1992; 65: 502-513 Google Scholar

  • [126] Cleland E.E., Chuine I., Menzel A., Mooney H.A., Schwartz M.D. Shifting plant phenology in response to global change. Trends Ecol Evol 2007; 22: 357-365 Google Scholar

  • [127] Poulin B., Lefebvre G., McNeil R. Tropical avian phenology in relation to abundance and exploitation of food resources. Ecology 1992; 73: 2295-2309 Google Scholar

  • [128] Galetti M. Diet of the scaly-headed parrot (Pionus maximiliani) in a semideciduous forest in southeastern Brazil. Biotropica 1993; 25: 419-425 Google Scholar

  • [129] Andelt W.F., Kie J.G., Knowlton F.F., Cardwell K. Variation in coyote diets associated with season and successional changes in vegetation. J Wildl Manage 1987; 51: 273-277 Google Scholar

  • [130] Cantu-Salazar L., Hidalgo-Mihart M.G., Lopez-Gonzalez C.A., Gonzalez-Romero A. Diet and food resource use by the pygmy skunk (Spilogale pygmaea) in the tropical dry forest of Chamela, Mexico. J Zool 2005; 267: 283-289 Google Scholar

  • [131] Cerling T.E., Viehl K. Seasonal diet changes of the forest hog (Hylochoerus meinertzhageni Thomas) based on the carbon isotopic composition of hair. Afr J Ecol 2004; 42: 88-92 Google Scholar

  • [132] Moran N.A., Hansen A.K., Powell J.E., Sabree Z.L. Distinctive gut microbiota of honey bees assessed using deep sampling from individual worker bees. PLoS One 2012; 7: e36393 Google Scholar

  • [133] King G.M., Judd C., Kuske C.R., Smith C. Analysis of stomach and gut microbiomes of the eastern oyster (Crassostrea virginica) from coastal Louisiana, USA. PLoS One 2012; 7: e51475 Google Scholar

  • [134] Kobayashi Y., Koike S., Miyaji M., Hata H., Tanaka K. Hingut microbes, fermentation and their seasonal variations in Hokkaido native horses compared to light horses. Ecological Research 2006; 21: 285-291 Google Scholar

  • [135] Amato K.R., Black howler monkey (Alouatta pigra) nutrition: Integrating the study of behavior, feeding ecology, and the gut microbial community. University of Illinois, Urbana, 2013 Google Scholar

  • [136] Chivers D.J., Hladik C.M., Diet and gut morphology in primates., Food acquisition and processing in primates, Springer, U.S.A., 1984: 213-230. Google Scholar

  • [137] Hume I.D., Warner A.C.I., Evolution of microbial digestion in mammals., Digestive physiology and metabolism in ruminants Springer, Netherlands, 1980 665-684. Google Scholar

  • [138] Hoverstad T., Midtvedt T. Short-chain fatty acids in germ free mice and rats. J Nutr 1986; 116: 1772-1776 Google Scholar

  • [139] Wostmann B.S., Larkin C., Moriarty A., Bruckner-Kardoss E. Dietary intake, energy metabolism, and excretory losses of adult male germfree Wistar rats. Lab Anim Sci 1983; 33: 46- 50 Google Scholar

  • [140] Backhed F., Ding H., Wang T., Hooper L.V., Koh G.Y., Nagy A., et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 2004; 101: 15718-15723 Google Scholar

  • [141] Crawford P.A., Crowley J.R., Sambandam N., Muegge B.D., Costello E.K., Hamady M., et al. Regulation of myocardial ketone body metabolism by the gut microbiota during nutrient deprivation. Proc Natl Acad Sci 2009; 106: 11276- 11281 Google Scholar

  • [142] Flint H.J., Duncan S.H., Scott K.P., Louis P. Interactions adn competition within the microbial community of the human colon: Links between diet and health. Environ Microbiol 2007; 9: 1101-1111 Google Scholar

  • [143] Samuel B.S., Gordon J.I. A humanized gnotobiotic mouse model of host-Archael-bacterial mutualism. Proc Natl Acad Sci USA 2006; 103: 10011-10016 Google Scholar

  • [144] Kanamori Y., Sugiyama M., Hashizume K., Yuki N., Morotomi M., Tanaka R. Experience of long-term synbiotic therapy in seven short bowel patients with refractory enterocolitis. Journal of Pediatric Surgery 2004; 39: 1686-1692 Google Scholar

  • [145] Pryde S.E., Duncan S.H., Hold G.H., Stewart C.S., Flint H.J. The microbiology of butyrate formation in the human colon. FEMS Microbiol Lett 2002; 217: 133-139 Google Scholar

  • [146] Bjorkholm B., Bok C.M., Lundin A., Rafter J., Hibberd M.L., Pettersson S. Intestinal microbiota regulate xenobiotic metabolism in the liver. PLoS One 2009; 4: e6958 Google Scholar

  • [147] Jackson R.L., Greiwe J.S., Schwen R.J. Emerging evidence of the health benefits of S-equol, an estrogen receptor beta agonist. Nutr Rev 2011; 69: 432-448 Google Scholar

  • [148] Santacruz A., Collado M.C., Garcia-Valdes L., Segura M.T., Martin-Lagos J.A., Anjos T., et al. Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. Br J Nutr 2010; 104: 83-92 Google Scholar

  • [149] Li M., Wang B., Zhang M., Rantalainen M., Wang S., Zhou H., et al. Symbiotic gut microbes modulate human metabolic phenotypes. Proc Natl Acad Sci USA 2008; 105: 2117-2122 Google Scholar

  • [150] Reddy B.S., Pleasants J.R., Wostmann B.S. Effect of intestinal microflora on iron and zinc metabolism, and on activities of metalloenzymes in rats. J Nutr 1972; 102: 101- 107 Google Scholar

  • [151] Milton K., Van Soest P., Robertson J. Digestive efficiencies of wild howler monkeys. Physiol Zoo 1980; 53: 402-409 Google Scholar

  • [152] Rosenfeld J.S. Functional redundancy in ecology and conservation. Oikos 2002; 98: 156 Google Scholar

  • [153] Kelly D., Campbell J.I., King T.P., Grant G., Jansson E.A., Coutts A.G.P., et al. Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shutting of PPAR-g and RelA. Nat Immun 2003; 5: 104-112 Google Scholar

  • [154] Fukuda S., Toh H., Hase K., Oshima K., Nakanishi Y., Yoshimura K., et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 2011; 469: 543-549 Google Scholar

  • [155] Smith K., McCoy K.D., Macpherson A.J. Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Seminars in immunology 2007; 19: 59-69 Google Scholar

  • [156] Mulder I.E., Schmidt B., Stokes C.R., Lewis M., Bailey M., Aminov R.I., et al. Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces. BMC Biol 2009; 7: 79 Google Scholar

  • [157] Koch H., Schmid-Hempel P. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc Natl Acad Sci USA 2001; 108: 19288-19292 Google Scholar

  • [158] Panigrahi A., Kiron V., Kobayashi T., Puangkaew J., Satoh S., Sugita H. Immune responses in rainbow trout Oncorhynchus mykiss induced by a potential probiotic bacteria Lactobacillus rhamnosus JCM 1136. Vet Immunol Immunop 2004; 102: 379-388 Google Scholar

  • [159] Balc’azar J.L., Vendrell D., de Blas I., Ruiz-Zarzuela I., Giron’es O., Muzquiz J.L. Immune modulation by probiotic strains: Quantification of phagocytosis of Aeromonas salmonicida by leukocytes isolated from gut of rainbow trout( Oncorhynchus mykiss) using a radiolabelling assay. Comp Immunol Microbiol 2006; 29: 335-343 Google Scholar

  • [160] Balc’azar J.L., de Blas I., Ruiz-Zarzuela I., Vendrell D., Calvo A.C., M’arquez I., et al. Changes in intestinal microbiota and humoral immune response following probiotic administration in brown trout (Salmo trutta). . Br J Nutr 2007; 97: 522-527 Google Scholar

  • [161] Irianto A., Austin B. Use of probiotics to control furunculosis in rainbow trout Oncorhynchus mykiss (Walbaum). Journal of Fish Disease 2002; 25: 333-342 Google Scholar

  • [162] Pirarat N., Kobayashi T., Katagiri T., Maita M., Endo M. Protective effects and mechanisms of a probiotic bacterium Lactobacillus rhamnosus against experimental Edwardsiella tarda infection in tilapia (Oreochromis niloticus). Vet Immunol Immunop 2006; 113: 339-347 Google Scholar

  • [163] Bauer E., Williams B.A., Smidt H., Verstegen M.W., Mosenthin R. Influence of the gastrointestinal microbiota on development of the immune system in young animals. Curr Issues Intest Microbiol 2006; 7: 35-51 Google Scholar

  • [164] Falk P.G., Hooper L.V., Midtvedt T., Gordon H.A. Creating and maintaining the gastrointestinal ecosystem: What we know and need to know from gnotobiology. Microbiol Mol Biol Rev 1998; 62: 1157-1170 Google Scholar

  • [165] Macpherson A.J., Harris N.L. Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 2004; 4: 478-485 Google Scholar

  • [166] Pollard M., Sharon N. Responses of Peyer’s patches in germfree mice to antigenic stimulation. Infect Immun 1970; 2: 96- 100 Google Scholar

  • [167] Glaister J.R. Factors affecting the lymphoid cells in the small intestinal epithelium of the mouse. Int Arch Allergy Appl Immunol 1973; 45: 719-730 Google Scholar

  • [168] Umesaki Y., Setoyama H., Matsumoto S., Okada Y. Expansion of alpha beta T-cell receptor-bearing intestinal intrepithelial lymphocytes after microbial colonization in germ-free mice and its independence from thymus. Immunology 1993; 79: 32-37 Google Scholar

  • [169] Imaoka A., Matsumoto S., Setoyama H., Okada Y., Umesaki Y. Proliferative recruitment of intestinal intraepithelial lymphocytes after microbial colonization of germ-free mice. Eur J Immunol 1996; 26: 945-948 Google Scholar

  • [170] Round J.L., Mazmanian S.K. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 2009; 9: 313-323 Google Scholar

  • [171] Lundin A., Bok C.M., Aronsson L., Bjorkholm B., Gustafsson J.A., Pott S., et al. Gut flora, Toll-like receptors and nuclear receptors: A tripartite communication that tunes innate immunity in large intestine. Cell Microbiol 2008; 10: 1093- 1103 Google Scholar

  • [172] Matsumoto S., Setoyama H., Umesaki Y. Differential induction of major histocompatability complex molecules on mouse intestine by bacterial colonization. Gastroenterol 1992; 103: 1777-1782 Google Scholar

  • [173] Umesaki Y., Okada Y., Matsumoto S., Imaoka A., Setoyama H. Segmented filamentous bacteria are indigenous intestinal bacteria that activate intraepithelial lymphocytes and induce MHC class II molecules and fucosyl asialo GM1 glycolipids on the small intestinal epithelial cells in the ex germ-free mouse. Microbiol Immunol 1995; 39: 555-562 Google Scholar

  • [174] Rakoff-Nahoum S., Paglino S., Eslami-Varzaneh F., Edberg S., Medzhitoz R. Recognition of commensal microflora by Toll-like receptors is required for intestinal homeostasis. Cell 2004; 118: 229-241 Google Scholar

  • [175] Gaboriau-Routhiau V., Rakotobe S., Lecuyer E., Mulder I.E., Lan A., Bridonneau C., et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 2009; 31: 677-689 Google Scholar

  • [176] Round J.L., Mazmanian S.K. Inducible Fox p3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci USA 2010; 107: 12204-12209 Google Scholar

  • [177] Neiss J.H., Leithauser F., Adler G., Reimann J. Commensal gut flora drives the expansion of proinflammatory CD4 T cells in the colonic lamina propria under normal and inflammatory conditions. J Immunol 2008; 180: 559-568 Google Scholar

  • [178] Hall J.A., Bouladoux N., Sun C.M., Wohlfert E.A., Blank R.B., Zhu Q., et al. Commensal DNA limits regulatory T cell conversion and is a natural adjuvant of intestinal immune responses. Immunity 2008; 29: 637-649 Google Scholar

  • [179] O’Mahony C., Scully P., O’Mahony D., Murphy S., O’Brien F., Lyons A., et al. Commensal-induced regulatory T cells mediate protection against pathogen-stimulated NF-KB activation. PLoS Pathogens 2008; 4: e1000112 Google Scholar

  • [180] Ivanov I.I., Atarashi K., Manel N., Brodie E.L., Shima T., Karaoz U., et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009; 139: 485-498 Google Scholar

  • [181] Atarashi K., Nishimura A., Shima T., Umesaki Y., Yamamoto M., Onoue M., et al. ATP drives lamina propria T(H)17 cell differentiation. Nature 2008; 455: 808-812 Google Scholar

  • [182] Wen L., Ley R.E., Volchkov P.Y., Stranges P.B., Avanesyan L., Stonebraker A.C., et al. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 2008; 455: 1109-1113 Google Scholar

  • [183] Macpherson A.J., McCoy K.D., Johansen F.E., Brandtzaeg P. The immune geography of IgA induction and function. Nat Rev 2008; 1: 11-22 Google Scholar

  • [184] Benveniste J., Lespinats G., Salomon J.C. Serum and secretory IgA in axenic and holoxenic mice. J Immunol 1971; 108: 1656-1662 Google Scholar

  • [185] Benveniste J., Lespinats G., Adam C., Salomon J.C. Immunoglobulins in intact, immunized, and contaminated axenic mice: Study of serum IgA. J Immunol 1971; 107: 1647-1655 Google Scholar

  • [186] Talham G.L., Jiang H.Q., Bos N.A., Cebra J.J. Segmented filamentous bacteria are potent stimuli of a physiologically normal state of the murine gut mucosal immune system. Infect Immun 1999; 67: 1992-2000 Google Scholar

  • [187] Noverr M.C., Huffnagle G.B. Does the microbiota regulate immune responses outside the gut? Trends Microbiol 2004; 12: 562-568 Google Scholar

  • [188] Mazmanian S.K., Liu C.H., Tzianabos A.O., Kasper D.L. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 2005; 122: 107- 118 Google Scholar

  • [189] Hansen C.H.F., Nielsen D.S., Kverka M., Zakostelska Z., Klimesova K., Hudcovic T., et al. Patterns of early gut colonization shape future immune responses of the host. PLoS One 2012; 7: e34043 Google Scholar

  • [190] Ichinohe T., Pang I.K., Kumamoto Y., Peaper D.R., Ho J.H., Murray T.S., et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc Natl Acad Sci USA 2011; 108: 5354-5359 Google Scholar

  • [191] Kim D.H., Austin B. Innate immune responses in rainbow trout (Oncorhynchus mykiss, Walbaum) induced by probiotics. Fish Shellfish Immunol 2006; 21: 513-524 Google Scholar

  • [192] Balc’azar J.L., de Blas I., Ruiz-Zarzuela I., Vendrell D., Giron’es O., Muzquiz J.L. Enhancement of the immune response and protection induced by probiotic lactic acid bacteria against furunculosis in rainbow trout (Oncorhynchus mykiss). FEMS Immunol Med Microbiol 2007; 51: 185-193 Google Scholar

  • [193] Nikoskelainen S., Ouwehand A.C., Bylund G., Salminen S., Lilius E.M. Immune enhancement in rainbow trout (Oncorhynchus mykiss) by potential probiotic bacteria (Lactobacillus rhamnosus). Fish Shellfish Immunol 2003; 15: 443-452 Google Scholar

  • [194] Strachan D.P. Hay fever, hygiene, and household size. BMJ 1989; 299: 1259-1260 Google Scholar

  • [195] Okada H., Kuhn C., Feillet H., Bach J.-F. The ‘hygiene hypothesis’ for autoimmune and allergic diseases: An update. Clin Exp Immunol 2010; 160: 1-9 Google Scholar

  • [196] von Mutius E., Vercelli D. Farm living: Effects on childhood asthma and allergy. Nat Rev Immunol 2010; 10: 861-868 Google Scholar

  • [197] Olszak T., An D., Zeissig S., Vera M.P., Richter J.E., Franke A., et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science 2012; 336: 489-493 Google Scholar

  • [198] Wikoff W.R., Anfora A.T., Liu J., Schultz P.G., Lesley S.A., Peters E.C., et al. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci USA 2009; 106: 3698-3703 Google Scholar

  • [199] Devkota S., Wang Y., Musch M.W., Leone V., Fehlner-Peach H., Nadimpalli A., et al. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice. Nature 2012; 487: 104-108 Google Scholar

  • [200] Kassinen A., Krogius-Kurikka L., Makivuokko H., Rinttila T., Paulin L., Corander J., et al. The fecal microbiota of irritable bowel syndrome patients differs significantly from that of healthy subjects. Gastroenterol 2007; 133: 24-33 Google Scholar

  • [201] Ley R.E., Turnbaugh P.J., Klein S., Gordon J.I. Human gut microbes associated with obesity. Nature 2006; 444: 1022- 1023 Google Scholar

  • [202] Hayes K.S., Bancroft M., Goldrick M., I. P., Roberts I.S., Grencis R.K. Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris. Science 2010; 328: 1391-1394 Google Scholar

  • [203] Martinez-Mota R., Valdespino C., Sanchez-Ramos M.A., Serio-Silva J.C. Effects of forest fragmention on the physiological stress of black howler monkeys. Anim Cons 2007; 10: 374-379 Google Scholar

  • [204] Trejo-Macias G., Estrada A.E., Mosqueda Cabrera M.A. Survey of helminth parasites in populations of Alouatta palliata mexicana and A. pigra in continuous and in fragmented habitat in Southern Mexico. Int J Primatol 2007; 28: 931-945 Google Scholar

  • [205] Gillespie T.R., Chapman C.A. Forest fragmentation, the decline of an endangered primate ,and changes in hostparasite interactions relative to an unfragmented forest. Am J Primatol 2008: 222-230 Google Scholar

  • [206] Mulvey M., Aho J.M., Lydeard C., Leberg P.L., Smith M.H. Comparative population genetic structure of a parasite (Fascioloides magna) and its definitive host. Evolution 1991; 45: 1628-1640 Google Scholar

  • [207] Carey C. Hypothesis concerning the disappearance of boreal toads from the mountains of Colorado. Conserv Biol 1993; 7: 355-362 Google Scholar

  • [208] Hudson P.J., Dobson A.P., Lafferty K.D. Is a healthy ecosystem one that is rich in parasites? Trends Ecol Evol 2006; 21: 382-385 Google Scholar

  • [209] Heijtz R.D., Wang S., Anuar F., Qian Y., Bjorkholm B., Samuelsson A., et al. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci USA 2011; 108: 3047-3052 Google Scholar

  • [210] Neufeld K.M., Kang N., Bienenstock J., Foster J.A. Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterology and Motility 2011; 23: 255-264 Google Scholar

  • [211] Messaoudi M., Lalonde R., Violle N., Javelot H., Desor D., Nejdi A., et al. Assessment of psychotropic-like properties of a probiotic fomulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br J Nutr 2010; 105: 755-764 Google Scholar

  • [212] Rao A.V., Bested A.C., Beaulne T.M., Katzman M.A., Iorio C., Berardi J.M., et al. A randomized, double-blind, placebocontrolled pilot study of a probiotic in emotional symptoms of chronic fatigue syndrome. Gut Pathogens 2009; 1: 6 Google Scholar

  • [213] Bravo J.A., Forsythe P., Chew M.V., Escaravage E., Savignac H.M., Dinan T.G., et al. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci USA 2011; 108: 16050-16055 Google Scholar

  • [214] Gareau M.G., Jury J., MacQueen G., Sherman P.M., Perdue M.H. Probiotic treatment of rat pups normalises corticosterone release and ameliorates colonic dysfunction induced by maternal separation. Gut 2007; 56: 1522-1528 Google Scholar

  • [215] Desbonnet L., Garrett L., Clarke G., Kiely B., Cryan J.F., Dinan T. Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience 2010; 170: 1179-1188 Google Scholar

  • [216] Bercik P., Verdu E.F., Foster J.A., Macri J., Potter M., Huang X., et al. Chronic gastrointestinal inflammation induces anxiety-like behavior and alters central nervous sytem biochemistry in mice. Gastroenterol 2010; 139: 2102-2112 Google Scholar

  • [217] Bercik P., Park A.J., Sinclair D., Khoshdel A., Lu J., Huang X., et al. The anxiolytic effect of Bifidobacterium longum NCC3001 involves vagal pathways for gut-brain communication. Neurogastroenterology and Motility 2011; 23: 1132-1139 Google Scholar

  • [218] Foster J.A., McVey Neufeld K.A. Gut-brain axis: How the microbiome influences anxiety and depression. Cell 2013; 36: 305-312 Google Scholar

  • [219] Saulnier D.M., Ringel Y., Heyman M.B., Foster J.A., Bercik P., Shulman R.J., et al. The intestinal microbiome, probiotics and prebiotics in neurogastroenterology. Landes Bioscience 2012; 4: 17-27 Google Scholar

  • [220] McVey Neufeld K.A., Mao Y.K., Bienenstock J., Foster J.A., Kunze W. The microbiome is essential for normal gut intrinsic primary afferent neuron excitability in the mouse. Neurogastroent Motil 2013; 25: 183-188 Google Scholar

  • [221] Kunze W., Mao Y.K., Wang B., Huizinga J.D., Ma F., Forsythe P., et al. Lactobacillus reuteri enhances excitability of colonic AH neurons by inhibiting calcium-dependent potassium channel opening. J Cell Mol Med 2009; 13: 2261-2270 Google Scholar

  • [222] Hanstock T.L., Clayton E.H., Li K.M., Mallet P.E. Anxiety and aggression associated with the fermentation of carbohydrates in the hindguts of rats. Physiol Behav 2004; 82: 357-368 Google Scholar

  • [223] Dantzer R., O’Connor J.C., Freund G.G., Johnson R.W., Kelley K.W. From inflammation to sickness and depression: When the immune system subjugates the brain. Nat Rev Neurosci 2008; 9: 46-56 Google Scholar

  • [224] Sokol H., Pigneur B., Watterlot L., Lakhdari O., Bermudez- Humaran L.G., Gratadoux J.J., et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 2008; 105: 16731-16736 Google Scholar

  • [225] Benton D. The influence of dietary status on the cognitive performance of children. Mol Nutr Food Res 2010; 54: 457- 470 Google Scholar

  • [226] Collado M., Isolauri E., Laitinen K., Salminen S. Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women. Am J Clin Nutr 2008; 88: 894- 899 Google Scholar

  • [227] Gutbrod T., Wolke D., Soehne B., Ohrt B., Riegel K. Effects of gestation and birth weight on the growth and development of very low birthweight small for gestational age infants: A matched group comparison. Arch Dis Child Fetal Neonatal Ed 2000; 82: F208-F214 Google Scholar

  • [228] Girard S.A., Bah T.M., Kaloustian S., Lada-Moldovan L., Rondeau I., Tompkins T.A., et al. Lactobacillus helveticus and Bifidobacterium longum taken in combination reduce the apoptosis propensity in the limbic system after myocardial infarction in a rat model. Br J Nutr 2009; 102: 1420-1425 Google Scholar

  • [229] Behie A.M., Pavelka M.S. The short-term effects of a hurricane on the diet and activity of black howlers (Alouatta pigra) in Monkey River, Belize. Folia Primatologia 2005; 76: 1-9 Google Scholar

  • [230] Chaves O.M., Stoner K.E., Arroyo-Rodriguez V. Seasonal differences in activity patterns of Geoffroyi’s spider monkeys (Ateles geoffroyi) living in continuous and fragmented forests in southern Mexico. Int J Primatol 2011; 32: 960-973 Google Scholar

  • [231] Overdorff D.J., Strait S.G., Telo A. Seasonal variation in activity and diet in a small-bodied folivorous primate, Hapalemur griseus, in southeastern Madagascar. Am J Primatol 1997; 43: 211-223 Google Scholar

  • [232] Ables E.D. Activity studies of red foxes in southern Wisconsin. J Wildl Manage 1969: 145-153 Google Scholar

  • [233] Relyea R.A. Activity of desert mule deer during the breeding season. J Mammal 1994: 940-949 Google Scholar

  • [234] Martin J., Lopez P. Social status of male Iberian rock lizards (Lacerta monticola) influences their activity patterns during the mating season. Can J Zool 2000; 78: 1105-1109 Google Scholar

  • [235] Baker-Henningham H., Hamadani J.D., Huda S.N., Grantham-McGregor S.M. Undernourished children have different temperaments than better-nourished children in rural Bangladesh. J Nutr 2009; 139: 1765-1771 Google Scholar

  • [236] Janson C.H. Testing the predation hypothesis for vertebrate sociality: Prospects and pitfalls. Behaviour 1998; 135: 389- 410 Google Scholar

  • [237] Hill R.A., Dunbar R.I.M. An evaluation of the roles of predation rate and predation risk as selective pressures on primate grouping behavior. Behaviour 1998; 135: 411-430 Google Scholar

  • [238] Alexander R.D. The evolution of social behavior. Ann Rev Ecol Syst 1974; 5: 325-383 Google Scholar

  • [239] Wilson E.O., Sociobiology. Harvard University Press, Cambridge, 1980 Google Scholar

  • [240] Clark C., Mangel M. The evolutionary advantages of group foraging. Theor Pop Biol 1986; 30: 45-75 Google Scholar

  • [241] Bergmuller R., Animal personality and behavioural syndromes., Animal Behaviour: Evolution and Mechanisms Springer, Berlin, 2010 587-621. Google Scholar

  • [242] Sih A., Bell A.M., Johnson J.C. Behavioral syndromes: An ecological and evolutionary overview. Trends Ecol Evol 2004; 19: 372-378 Google Scholar

  • [243] Clark A., Ehlinger T.J. Pattern and adaptation in individual behavioral differences. Perspectives in Ethology 1987; 7: 1-47 Google Scholar

  • [244] Sih A., Bell A.M., Insights for behavioral ecology from behavioral syndromes., Advances in the Study of Behavior2008 227-281. Google Scholar

  • [245] Frost A.J., Winrow-Giffen A., Ashley P.J., Sneddon L.U. Plasticity in animal personality traits: Does prior experience alter the degree of boldness? Proc Royal Soc B 2007; 274: 333-339 Google Scholar

  • [246] Bell A.M., Sih A. Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett 2007; 10: 828-834 Google Scholar

  • [247] Bergmuller R., Taborsky M. Animal personality due to social niche specialisation. Trends Ecol Evol 2010; 25: 504-511 Google Scholar

  • [248] Careau V., Thomas D., Humphries M.M., Reale D. Energy metabolism and animal personality. Oikos 2008; 117: 642- 653 Google Scholar

  • [249] Biro P.A., Stamps J.A. Are animal personality traits linked to life-history productivity? Trends Ecol Evol 2008; 23: 361-368 Google Scholar

  • [250] Stamps J.A. Growth-mortality tradeoffs and ‘personality traits’ in animals. Ecol Lett 2007; 10: 355-363 Google Scholar

  • [251] Dingemanse N.J., Both C., Drent P.J., Tinbergen J.M. Fitness consequences of avian personalities in a fluctuating environment. Proc Royal Soc B 2004; 271: 847-852 Google Scholar

  • [252] Wilson A.D.M., Godin J.-G.J., Ward J.W. Boldness and reproductive fitness correlates in the Eastern mosquitofish, Gambusia holbrooki. Ethology 2009; 116: 96-104 Google Scholar

  • [253] Bailey M., Coe C.L. Maternal separation disrupts the integrity of the intestingal micoflora in infant rhesus monkeys. Dev Psychobiol 1999; 35: 146-155 Google Scholar

  • [254] Suzuki K., Harasawa R., Yoshitake Y., Mitsuoka T. Effect of crowding and heat stress on intestinal flora, body weight gain, and feed efficiency of growing rats and chicks. Nippon Juigaku Zasshi 1983; 45: 331-338 Google Scholar

  • [255] Xu J., Mahowald M.A., Ley R.E., Lozupone C., Hamady M., Martens E.C., et al. Evolution of symbiotic bacteria in the distal human intestine. PLoS Biol 2007; 5: e156 Google Scholar

  • [256] Mackie R.I. Mutualistic fermentative digestion in the gastrointestinal tract: Diversity and evolution. Integr Comp Biol 2002; 42: 319-326 Google Scholar

  • [257] Benezra A., DeStefano J., Gordon J.I. Anthropology of microbes. Proc Natl Acad Sci USA 2012; 109: 6378-6381 Google Scholar

  • [258] Ochman H., Worobey M., Kuo C.H., Ndjango J.B.N., Peeters M., Hahn B.H., et al. Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol 2010; 8: e1000546 Google Scholar

  • [259] Yildirim S., Yeoman C.J., Sipos M., Torralba M., Wilson B.A., Goldberg T.L., et al. Characterization of the fecal microbiome from non-human wild primates reveals species specific microbial communities. PLoS One 2010; 5: e13963 Google Scholar

  • [260] Xu J., Gordon J.I. Honor thy symbionts. PNAS 2003; 100: 10452-10459 Google Scholar

  • [261] Zaneveld J., Turnbaugh P.J., Lozupone C., Ley R.E., Hamady M., Gordon J.I., et al. Host-bacterial coevolution and the search for new drug targets. Curr Opin Chem Biol 2008; 12: 109-114 Google Scholar

  • [262] Strier K.B., Boubli J.P. A history of long-term research and conservation of northern muriquis (Brachyteles hypoxanthus) at the Estacao Biologica de Caratinga/RPPN-FMA. Primate Conservation 2006; 20: 53-63 Google Scholar

  • [263] Alberts S.C., Watts H.E., Altmann J. Queuing and queuejumping: Long-term patterns of reproductive skew in male savannah baboons, Papio cynocephalus. Anim Behav 2003; 65: 821-840 Google Scholar

  • [264] Pusey A.E., Pintea L., Wilson M.L., Shadrack K., Goodall J. The contribution of long-term research at Gombe National Park to chimpanzee conservation. Conserv Biol 2007; 21: 623-634 Google Scholar

  • [265] Koenig A., Borries C., Social organization and male residence pattern in Phayre’s leaf monkeys., In: Kappeler PM, Watts DP, (Eds.), Long-term Field Studies of Primates, Springer, Berlin Heidelberg, Heidelberg, 2012: 215-236. Google Scholar

  • [266] Skelly D.K., Werner E.E., Cortwright S.A. Long-term distributional dynamics of a Michigan amphibian assemblage. Ecology 1999; 80: 2326-2337 Google Scholar

  • [267] Holmes R.T., Sherry T.W., Sturges S.W. Bird community dynamics in a temperate deciduous forest: Long-term trends at Hubbard Brook. Ecol Monogr 1986; 56: 201-220 Google Scholar

  • [268] Durant S.M., Bashir S., Maddox T., Laurenson K. Relating long-term studies to conservation practice: The case of the Serengeti Cheetah Project. Conserv Biol 2007; 21: 602-611 Google Scholar

  • [269] Clutton-Brock T., Sheldon B.C. Individuals and populations: The role of long-term, individual-based studies of animals in ecology and evolutionary biology. Trends Ecol Evol 2010; 25: 562-573 Google Scholar

  • [270] Petit S., Waudby H.P., Walker A.T., Zanker R., Rau G. A non-mutilating method for marking small wild mammals and reptiles. Aust J Zool 2012; 60: 64-71 Google Scholar

  • [271] Pagano A.M., Peacock E., McKinney M.A. Remote biopsy darting and marking of polar bears. Mar Mammal Sci 2013; doi: 10.1111/mms.12029 CrossrefGoogle Scholar

  • [272] Sikes R.S., Gannon W.L. Guidelines of the American Society of Mammologists for the use of wild mammals in research. J Mammal 2011; 92: 235-253 Google Scholar

  • [273] Knights D., Kuczynski J., Charlson E.S., Zaneveld J., Mozer M.C., Collman R.G., et al. Bayesian communitywide culture-independent microbial source tracking. Nat Methods 2011; 8: 761-763 Google Scholar

  • [274] Wu G.D., Lewis J.D., Hoffman C., Chen Y.Y., Knight R., Bittinger K., et al. Sampling and pyrosequencing methods for characterizing bacterial communities in the human gut using 16S sequence tags. BMC Microbiol 2010; 10: 206 Google Scholar

  • [275] Vlckova K., Mrazek J., Kopecny J., Petrzelkova K.J. Evaluation of different storage methods to characterize the fecal bacterial communities of captive western lowland gorillas (Gorilla gorilla gorilla). J Microbiol Methods 2012; 91: 45-51 Google Scholar

  • [276] Pakpour S., Milani A.S., Chenier M.R. A multi-criteria decision-making approach for comparing sample preservation and DNA extraction methods from swine feces. Am J Mol Biol 2012; 2: 159-169 Google Scholar

  • [277] Rossmanith P., Roder B., Fruhwirth K., Vogl C. Mechanisms of degradation of DNA standards for calibration function during storage. Appl Microbiol Biotechnol 2011; 89: 407- 417 Google Scholar

  • [278] Gray M.A., Pratte Z.A., Kellogg C.A. Comparison of DNA preservation methods for environmental bacterial community samples. FEMS Microb Ecol 2012; 83: 468- 477 Google Scholar

  • [279] Deevong P., Hongoh Y., Inoue T., Trakulnaleamsai S., Kudo T., Noparatnaraporn N., et al. Effect of temporal sample preservation on the molecular study of a complex microbial community in the gut of the termite Microcerotermes sp. Microbes Environ 2006; 21: 78-85 Google Scholar

  • [280] Simister R.L., Schmitt S., Taylor M.W. Evaluating methods for the preservation and extraction of DNA and RNA for analysis of microbial communities in marine sponges. J Exp Mar Biol Ecol 2011; 397: 38-43 Google Scholar

  • [281] Nechvatal J.M., Ram J.L., Basson M.D., Namprachan P., Niec S.R., Badsha K.Z., et al. Fecal collection, ambient preservation, and DNA extraction for PCR amplification of bacterial and human markers from human feces. J Microbiol Methods 2008; 72: 124-132 Google Scholar

  • [282] Moreau C.S., Wray B.D., Czekanski-Moir J.E., Rubin B.E.R. DNA preservation: A test of commonly used preservatives for insects. Invertebr Syst 2013; 27: 81-86 Google Scholar

  • [283] Koren O., Goodrich J.K., Cullender T.C., Spor A., Laitinen K., Backhed H.K., et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 2012; 150: 470-480 Google Scholar

  • [284] Kitaysky A.S., Wingfield J.C., Piatt J.F. Dynamics of food availability, body condition and physiological stress response in breeding Black-legged Kittiwakes. Funct Ecol 2002; 13: 577-584 Google Scholar

  • [285] Chapman C.A., Saj T.L., Snaith T.V. Temporal dynamics of nutrition, parasitism, and stress in colobus monkeys: implications for population regulation and conservation. Am J Physiol Anthr 2007: 240-250 Google Scholar

  • [286] Kotrschal K., Hirschenhauser K., Mostl E. The relationship between social stress and dominance is sesaonal in greylag geese. Animal Behaviour 1998; 55: 171-176 Google Scholar

  • [287] Romero L.M. Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen Comp Endocrinol 2002; 128: 1-24 Google Scholar

About the article


Received: 2013-08-05

Accepted: 2013-09-29

Published Online: 2013-10-22


Citation Information: Microbiome Science and Medicine, ISSN (Online) 2084-7653, DOI: https://doi.org/10.2478/micsm-2013-0002.

Export Citation

©2013 Versita Sp. z o.o.. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

[1]
Wasimuddin, Sebastian Menke, Jörg Melzheimer, Susanne Thalwitzer, Sonja Heinrich, Bettina Wachter, and Simone Sommer
Molecular Ecology, 2017
[2]
Molly C. Bletz, Holly Archer, Reid N. Harris, Valerie J. McKenzie, Falitiana C. E. Rabemananjara, Andolalao Rakotoarison, and Miguel Vences
Frontiers in Microbiology, 2017, Volume 8
[3]
Emily L Pascoe, Heidi C Hauffe, Julian R Marchesi, and Sarah E Perkins
The ISME Journal, 2017
[4]
Dan Xue, Huai Chen, Xinquan Zhao, Shixiao Xu, Linyong Hu, Tianwei Xu, Lin Jiang, and Wei Zhan
Systematic and Applied Microbiology, 2017, Volume 40, Number 4, Page 227
[5]
Huan Li, Tongtong Li, Bo Tu, Yongping Kou, and Xiangzhen Li
Applied Microbiology and Biotechnology, 2017, Volume 101, Number 13, Page 5519
[6]
Tongtong Li, Meng Long, Huan Li, François-Joël Gatesoupe, Xujie Zhang, Qianqian Zhang, Dongyue Feng, and Aihua Li
Frontiers in Microbiology, 2017, Volume 8
[7]
Timothy J. Colston
Molecular Ecology, 2017, Volume 26, Number 4, Page 972
[9]
Jakub Kreisinger, Lucie Kropáčková, Adéla Petrželková, Marie Adámková, Oldřich Tomášek, Jean-François Martin, Romana Michálková, and Tomáš Albrecht
Frontiers in Microbiology, 2017, Volume 8
[10]
Elizabeth A. Miller, Joshua A. Livermore, Susan C. Alberts, Jenny Tung, and Elizabeth A. Archie
Microbiome, 2017, Volume 5, Number 1
[11]
Randall R. Jiménez and Simone Sommer
Biodiversity and Conservation, 2017, Volume 26, Number 4, Page 763
[12]
Tiantian Ren, Ariel F. Kahrl, Martin Wu, and Robert M. Cox
Molecular Ecology, 2016, Volume 25, Number 19, Page 4793
[13]
Timothy J. Colston and Colin R. Jackson
Molecular Ecology, 2016, Volume 25, Number 16, Page 3776
[14]
Dan Xue, Huai Chen, Fang Chen, Yixin He, Chuan Zhao, Dan Zhu, Lile Zeng, and Wei Li
Livestock Science, 2016, Volume 188, Page 61
[15]
Joanna E. Lambert and Jessica M. Rothman
Annual Review of Anthropology, 2015, Volume 44, Number 1, Page 493
[16]
Jakub Kreisinger, Géraldine Bastien, Heidi C Hauffe, Julian Marchesi, and Sarah E Perkins
Philosophical Transactions of the Royal Society B: Biological Sciences, 2015, Volume 370, Number 1675, Page 20140295
[17]
Tiantian Ren, Laura E. Grieneisen, Susan C. Alberts, Elizabeth A. Archie, and Martin Wu
Environmental Microbiology, 2016, Volume 18, Number 5, Page 1312
[18]
Carlos Magno da Costa Maranduba, Sandra Bertelli Ribeiro De Castro, Gustavo Torres de Souza, Cristiano Rossato, Francisco Carlos da Guia, Maria Anete Santana Valente, João Vitor Paes Rettore, Claudinéia Pereira Maranduba, Camila Maurmann de Souza, Antônio Márcio Resende do Carmo, Gilson Costa Macedo, and Fernando de Sá Silva
Journal of Immunology Research, 2015, Volume 2015, Page 1
[19]
Sebastian Menke, Wasimuddin, Matthias Meier, Jörg Melzheimer, John K. E. Mfune, Sonja Heinrich, Susanne Thalwitzer, Bettina Wachter, and Simone Sommer
Frontiers in Microbiology, 2014, Volume 5

Comments (0)

Please log in or register to comment.
Log in