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An altered microbiome in urban coyotes mediates relationships between anthropogenic diet and poor health

  • 1.

    Foley, J. A. et al. Global consequences of land use. Science 309, 570–574 (2005).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 2.

    Ellis, E. C., Goldewijk, K. K., Siebert, S., Lightman, D. & Ramankutty, N. Anthropogenic transformation of the biomes, 1700 to 2000. Glob. Ecol. Biogeogr. 19, 589–606 (2010).

    Google Scholar 

  • 3.

    Concepción, E. D., Moretti, M., Altermatt, F., Nobis, M. P. & Obrist, M. K. Impacts of urbanisation on biodiversity: the role of species mobility, degree of specialisation and spatial scale. Oikos 124, 1571–1582 (2015).

    Article  Google Scholar 

  • 4.

    Lowry, H., Lill, A. & Wong, B. B. M. Behavioural responses of wildlife to urban environments. Biol. Rev. 88, 537–549 (2013).

    PubMed  Article  Google Scholar 

  • 5.

    Callaghan, C. T. et al. Generalists are the most urban-tolerant of birds: a phylogenetically controlled analysis of ecological and life history traits using a novel continuous measure of bird responses to urbanization. Oikos 128, 845–858 (2019).

    Article  Google Scholar 

  • 6.

    Ducatez, S., Sayol, F., Sol, D. & Lefebvre, L. Are urban vertebrates city specialists, artificial habitat exploiters, or environmental generalists? Integr. Comp. Biol. 58, 929–938 (2018).

    PubMed  Article  Google Scholar 

  • 7.

    Murray, M. H. et al. City sicker? A meta-analysis of wildlife health and urbanization. Front. Ecol. Environ. 17, 575–583 (2019).

    Article  Google Scholar 

  • 8.

    Lyons, J., Mastromonaco, G., Edwards, D. B. & Schulte-Hostedde, A. I. Fat and happy in the city: eastern chipmunks in urban environments. Behav. Ecol. 28, 1464–1471 (2017).

    Article  Google Scholar 

  • 9.

    Meillère, A. et al. Corticosterone levels in relation to trace element contamination along an urbanization gradient in the common blackbird (Turdus merula). Sci. Total Environ. 566–567, 93–101 (2016).

    ADS  PubMed  Article  CAS  Google Scholar 

  • 10.

    Soto-Calderón, I., Acevedo-Garcés, Y., Álvarez-Cardona, J., Hernandez, C. & García, G. Physiological and parasitological implications of living in a city: the case of the white-footed tamarin (Saguinus leucopus). Am. J. Primatol. 78, (2016).

  • 11.

    Sillero-Zubiri, C., Sukumar, R. & Treves, A. Living with wildlife: the roots of conflict and the solutions. In Key Topics in Conservation Biology (eds. MacDonald, D. & Service, K.) 255–272 (2006).

  • 12.

    Muegge, B. D. et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332, 970–974 (2011).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 13.

    Hanning, I. & Diaz-Sanchez, S. The functionality of the gastrointestinal microbiome in non-human animals. Microbiome 3, 51 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  • 14.

    Tremaroli, V. & Bäckhed, F. Functional interactions between the gut microbiota and host metabolism. Nature 489, 242–249 (2012).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 15.

    Pickard, J. M., Zeng, M. Y., Caruso, R. & Núñez, G. Gut microbiota: role in pathogen colonization, immune responses, and inflammatory disease. Immunol. Rev. 279, 70–89 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 16.

    Mockler, B. K., Kwong, W. K., Moran, N. A. & Koch, H. Microbiome structure influences infection by the parasite Crithidia bombi in bumble bees. Appl. Environ. Microbiol. 84, e02335-e2417 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  • 17.

    Suzuki, T. A. Links between natural variation in the microbiome and host fitness in wild mammals. Integr. Comp. Biol. 57, 756–769 (2017).

    CAS  PubMed  Article  Google Scholar 

  • 18.

    Kirchoff, N. S., Udell, M. A. & Sharpton, T. J. The gut microbiome correlates with conspecific aggression in a small population of rescued dogs (Canis familiaris). PeerJ 7, e6103 (2019).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 19.

    Walter, J. Ecological role of lactobacilli in the gastrointestinal tract: implications for fundamental and biomedical research. Appl. Environ. Microbiol. 74, 4985–4996 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 20.

    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 

  • 21.

    Murray, M. H. et al. Gut microbiome shifts with urbanization and potentially facilitates a zoonotic pathogen in a wading bird. PLoS ONE 15, 1–16 (2020).

    Google Scholar 

  • 22.

    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 

  • 23.

    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. 287, (2020).

  • 24.

    Stothart, M. R., Palme, R. & Newman, A. E. M. It’s what’s on the inside that counts: stress physiology and the bacterial microbiome of a wild urban mammal. Proc. R. Soc. B Biol. Sci. 286, (2019).

  • 25.

    Becker, C. G., Longo, A. V., Haddad, C. F. B. & Zamudio, K. R. Land cover and forest connectivity alter the interactions among host, pathogen and skin microbiome. Proc. R. Soc. B Biol. Sci. 284, 20170582 (2017).

    Article  Google Scholar 

  • 26.

    Bestion, E. et al. Climate warming reduces gut microbiota diversity in a vertebrate ectotherm. Nat. Ecol. Evol. 1, 0161 (2017).

    Article  Google Scholar 

  • 27.

    Barelli, C. et al. Habitat fragmentation is associated to gut microbiota diversity of an endangered primate: implications for conservation. Sci. Rep. 5, 14862 (2015).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 28.

    Trevelline, B. K., Fontaine, S. S., Hartup, B. K. & Kohl, K. D. Conservation biology needs a microbial renaissance: a call for the consideration of host-associated microbiota in wildlife management practices. Proc. R. Soc. B Biol. Sci. 286, (2019).

  • 29.

    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. 15, 1132–1145 (2013).

    CAS  PubMed  Article  Google Scholar 

  • 30.

    Wasimuddin, et al. Gut microbiomes of free-ranging and captive Namibian cheetahs: diversity, putative functions and occurrence of potential pathogens. Mol. Ecol. 26, 5515–5527 (2017).

    CAS  PubMed  Article  Google Scholar 

  • 31.

    Amato, K. R. et al. Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes. ISME J. 13, 576–587 (2019).

    CAS  PubMed  Article  Google Scholar 

  • 32.

    Gehrt, S. D. & Riley, S. P. D. Coyotes (Canis latrans). in Urban Carnivores: Ecology, Conflict, and Conservation (eds. Gehrt, S. D., Riley, S. P. D. & Cypher, B. L.) 79–95 (2010).

  • 33.

    Breck, S. W., Poessel, S. A., Mahoney, P. & Young, J. K. The intrepid urban coyote: a comparison of bold and exploratory behavior in coyotes from urban and rural environments. Sci. Rep. 9, 2104 (2019).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 34.

    Gier, H. T. Coyotes in Kansas. (1968).

  • 35.

    Murray, M. H. et al. Greater consumption of protein-poor anthropogenic food by urban relative to rural coyotes increases diet breadth and potential for human-wildlife conflict. Ecography 38, 001–008 (2015).

    Article  Google Scholar 

  • 36.

    Massolo, A., Liccioli, S., Budke, C. & Klein, C. Echinococcus multilocularis in North America: the great unknown. Parasite 21, 73 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  • 37.

    Murray, M. H., Edwards, M. A., Abercrombie, B. & St. Clair, C. C. Poor health is associated with use of anthropogenic resources in an urban carnivore. Proc. R. Soc. B Biol. Sci. 282, 20150009 (2015).

  • 38.

    Murray, M. H., Hill, J., Whyte, P. & St. Clair, C. C. Urban compost attracts coyotes, contains toxins, and may promote disease in urban-adapted wildlife. Ecohealth 13, 285–292 (2016).

  • 39.

    Luong, L. T., Chambers, J. L., Moizis, A., Stock, T. & St. Clair, C. Helminth parasites and zoonotic risk associated with urban coyotes (Canis latrans) in Alberta, Canada. J. Helminthol. 94, e25 (2020).

  • 40.

    Corbin, E. et al. Spleen mass as a measure of immune strength in mammals. Mamm. Rev. 38, 108–115 (2008).

    Article  Google Scholar 

  • 41.

    Newsome, S. D., Ralls, K., Van Horn Job, C., Fogel, M. L. & Cypher, B. L. Stable isotopes evaluate exploitation of anthropogenic foods by the endangered San Joaquin kit fox (Vulpes macrotis mutica). J. Mammol. 91, 1313–1321 (2010).

  • 42.

    Huot, J., Poulle, M. & Crate, M. Evaluation of several indices for assessment of coyote (Canis latrans) body composition. Can. J. Zool. 73, 1620–1624 (1995).

    Article  Google Scholar 

  • 43.

    Tucker, C. M. et al. A guide to phylogenetic metrics for conservation, community ecology and macroecology. Biol. Rev. 92, 698–715 (2016).

    PubMed  Article  Google Scholar 

  • 44.

    Reese, A. T. & Dunn, R. R. Drivers of microbiome biodiversity: a review of general rules, feces, and ignorance. MBio 9, e01294-e1318 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  • 45.

    Pilla, R. & Suchodolski, J. S. The role of the canine gut microbiome and metabolome in health and gastrointestinal disease. Front. Vet. Sci. 6, 498 (2020).

    PubMed  PubMed Central  Article  Google Scholar 

  • 46.

    Conlon, M. A. & Bird, A. R. The impact of diet and lifestyle on gut microbiota and human health. Nutrition 7, 17–44 (2015).

    Google Scholar 

  • 47.

    Makki, K., Deehan, E. C., Walter, J. & Bäckhed, F. The impact of dietary fiber on gut microbiota in host health and disease. Cell Host Microbe 23, 705–715 (2018).

    CAS  PubMed  Article  Google Scholar 

  • 48.

    Schnorr, S. L. et al. Gut microbiome of the Hadza hunter-gatherers. Nat. Commun. 5, 3654 (2014).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 49.

    Vieco-Saiz, N. et al. Benefits and inputs from lactic acid bacteria and their bacteriocins as alternatives to antibiotic growth promoters during food-animal production. Front. Microbiol. 10, 1–17 (2019).

    Article  Google Scholar 

  • 50.

    Karasov, W. H. & Douglas, A. E. Comparative digestive physiology. Comp. Physiol. 3, 741–783 (2013).

    Google Scholar 

  • 51.

    Wang, T. et al. Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J. 6, 320–329 (2012).

    CAS  PubMed  Article  Google Scholar 

  • 52.

    AlShawaqfeh, M. K. et al. A dysbiosis index to assess microbial changes in fecal samples of dogs with chronic inflammatory enteropathy. FEMS Microbiol. Ecol. 93, 1–8 (2017).

    Article  CAS  Google Scholar 

  • 53.

    Beldomenico, P. M. & Begon, M. Disease spread, susceptibility and infection intensity: vicious circles? Trends Ecol. Evol. 25, 21–27 (2010).

    PubMed  Article  Google Scholar 

  • 54.

    Newsome, S. D., Garbe, H. M., Wilson, E. C. & Gehrt, S. D. Individual variation in anthropogenic resource use in an urban carnivore. Oecologia 178, 115–128 (2015).

    ADS  PubMed  Article  Google Scholar 

  • 55.

    Henderson, G. et al. Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range. Sci. Rep. 5, 14567 (2015).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 56.

    Brennan, C. A. & Garrett, W. S. Fusobacterium nucleatum – symbiont, opportunist and oncobacterium. Nat. Rev. Microbiol. 17, 156–166 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 57.

    Bermingham, E. N., Maclean, P., Thomas, D. G., Cave, N. J. & Young, W. Key bacterial families (Clostridiaceae, Erysipelotrichaceae and Bacteroidaceae) are related to the digestion of protein and energy in dogs. PeerJ 5, e3019 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 58.

    Alessandri, G. et al. Metagenomic dissection of the canine gut microbiota: insights into taxonomic, metabolic and nutritional features. Environ. Microbiol. 21, 1331–1343 (2019).

    CAS  PubMed  Article  Google Scholar 

  • 59.

    Schmidt, M. et al. The fecal microbiome and metabolome differs between dogs fed Bones and Raw Food (BARF) diets and dogs fed commercial diets. PLoS ONE 13, e0201279 (2018).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 60.

    Sandri, M., Dal Monego, S., Conte, G., Sgorlon, S. & Stefanon, B. Raw meat based diet influences faecal microbiome and end products of fermentation in healthy dogs. BMC Vet. Res. 13, 1–11 (2017).

    Google Scholar 

  • 61.

    Moon, C. D., Cookson, A. L., Young, W., Maclean, P. H. & Bermingham, E. N. Metagenomic insights into the roles of Proteobacteria in the gastrointestinal microbiomes of healthy dogs and cats. Microbiologyopen 7, e677 (2018).

    Article  Google Scholar 

  • 62.

    Wu, X. et al. Analysis and comparison of the wolf microbiome under different environmental factors using three different data of next generation sequencing. Sci. Rep. 7, 11332 (2017).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 63.

    Wang, B. & Wang, X.-L. Species diversity of fecal microbial flora in Canis lupus familiaris infected with canine parvovirus. Vet. Microbiol. 237, 108390 (2019).

    PubMed  Article  Google Scholar 

  • 64.

    Chen, L. et al. NLRP12 attenuates colon inflammation by maintaining colonic microbial diversity and promoting protective commensal bacterial growth. Nat. Immunol. 18, 541–551 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 65.

    Martínez, I. et al. Gut microbiome composition is linked to whole grain-induced immunological improvements. ISME J. 7, 269–280 (2013).

    PubMed  Article  CAS  Google Scholar 

  • 66.

    Liu, Y. et al. Splenectomy leads to amelioration of altered gut microbiota and metabolome in liver cirrhosis patients. Front. Microbiol. 9, 1–13 (2018).

    Article  Google Scholar 

  • 67.

    Demas, G. E., Zysling, D. A., Beechler, B. R., Muehlenbein, M. P. & French, S. S. Beyond phytohaemagglutinin: assessing vertebrate immune function across ecological contexts. J. Anim. Ecol. 80, 710–730 (2011).

    PubMed  Article  Google Scholar 

  • 68.

    Sugden, S. A., St. Clair, C. C. & Stein, L. Y. Individual and site-specific variation in a biogeographical profile of the coyote intestinal microbiota. Microb. Ecol. (2020).

  • 69.

    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 

  • 70.

    Leung, J. M., Graham, A. L. & Knowles, S. C. L. Parasite-microbiota interactions with the vertebrate gut: synthesis through an ecological lens. Front. Microbiol. 9, 843 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  • 71.

    Ezenwa, V. O., Gerardo, N. M., Inouye, D. W., Medina, M. & Xavier, J. B. Animal behavior and the microbiome. Science 338, 198–199 (2012).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 72.

    Stewart, R. E. A., Stewart, B. E., Stirling, I. & Street, E. Counts of growth layer groups in cementum and dentine in ringed seals. Mar. Mammal Sci. 12, 383–401 (1996).

    Article  Google Scholar 

  • 73.

    Linhart, S. B. & Knowlton, F. F. Determining age of coyotes by tooth cementum layers. J. Wildl. Manage. 31, 362–365 (1967).

    Article  Google Scholar 

  • 74.

    Jahren, A. H. & Kraft, R. A. Carbon and nitrogen stable isotopes in fast food: signatures of corn and confinement. Proc. Natl. Acad. Sci. 105, 17855–17860 (2008).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 75.

    Parnell, A. C. simmr: a stable isotope mixing model. (2019).

  • 76.

    Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. 108, 4516–4522 (2011).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 77.

    Hsieh, T. C., Ma, K. H. & Chao, A. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol. Evol. 7, 1451–1456 (2016).

    Article  Google Scholar 

  • 78.

    Davis, N. M., Proctor, D. M., Holmes, S. P., Relman, D. A. & Callahan, B. J. Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome 6, 226 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  • 79.

    Trachsel, D., Deplazes, P. & Mathis, A. Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology 134, 911–920 (2007).

    CAS  PubMed  Article  Google Scholar 

  • 80.

    R Core Team. R: A language and environment for statistical computing. (2019).

  • 81.

    Chao, A. et al. Rarefaction and extrapolation of phylogenetic diversity. Methods Ecol. Evol. 6, 380–388 (2015).

    Article  Google Scholar 

  • 82.

    Kembel, S. et al. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26, 1463–1464 (2010).

    CAS  Article  Google Scholar 

  • 83.

    Giam, X. & Olden, J. D. Quantifying variable importance in a multimodel inference framework. Methods Ecol. Evol. 7, 388–397 (2016).

    Article  Google Scholar 

  • 84.

    Cade, B. S. Model averaging and muddled multimodel inferences. Ecology 96, 2370–2382 (2015).

    PubMed  Article  Google Scholar 

  • 85.

    Fernandes, A., Macklaim, J. M., Linn, T., Reid, G. & Gloor, G. B. ANOVA-like differential expression (ALDEx) analysis for mixed population RNA-Seq. PLoS ONE 8, e67019 (2013).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 


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