Abstract
The gut microbiome is gaining recognition for its role in primate nutrition, but we stand to benefit from microbiome comparisons across diverse hosts and environmental conditions. We compared gut microbiome structure in four lemur species from four phylogenetic lineages, including 9 individual mouse lemurs (Microcebus danfossi), 6 brown lemurs (Eulemur fulvus), 20 sifakas (Propithecus coquereli), and a single sportive lemur (Lepilemur grewcockorum). In northwestern Madagascar, these species are sympatric, but use different feeding strategies to cope with environmental challenges, including relying on tree gums and insects (mouse lemurs), and some vs. significant leaf matter (brown lemurs vs. sifakas and sportive lemurs). From one fecal sample collected per lemur in the dry season in the Anjajavy Forest, we determined gut microbiome diversity, variability, and membership via 16S rRNA sequencing. The lemurs harbored strongly species-specific gut microbiomes. Brown lemurs showed more diverse and generalized consortia; mouse lemurs, sifakas, and the sportive lemur had less diverse consortia with more distinct memberships. Consistent with their fallback foods, mouse lemur microbiomes included taxa putatively associated with gum and insect digestion, whereas those of sifakas and the sportive lemur showed stronger and distinct signatures of leaf fiber and secondary compound metabolism. These results point to feeding strategy, intertwined with host phylogeny, as a driver of gut microbiome composition, but highlight real-time dietary specificity as a contributing driver of microbiome diversity. While illuminating how gut microbiomes facilitate host nutrition on challenging foods, these results help explain how ecologically diverse primates living in sympatry may differentially cope with seasonal or stochastic lean times.
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References
Aivelo, T., Laakkonen, J., & Jernvall, J. (2016). Population-and individual-level dynamics of the intestinal microbiota of a small primate. Applied and Environmental Microbiology, 82, 3537–3545. https://doi.org/10.1128/AEM.00559-16.
Alarifi, S., Bell, A., & Walton, G. (2018). In vitro fermentation of gum acacia: Impact on the faecal microbiota. International Journal of Food Sciences and Nutrition, 69, 696–704.
Alberdi, A., Aizpurua, O., Bohmann, K., Zepeda-Mendoza, M. L., & Gilbert, M. T. P. (2016). Do vertebrate gut metagenomes confer rapid ecological adaptation? Trends in Ecology & Evolution, 31, 689–699. https://doi.org/10.1016/j.tree.2016.06.008.
Amato, K. R., Leigh, S. R., Kent, A., Mackie, R. I., Yeoman, C. J., Stumpf, R. M., Wilson, B. A., Nelson, K. E., White, B. A., & Garber, P. A. (2015). The gut microbiota appears to compensate for seasonal diet variation in the wild black howler monkey (Alouatta pigra). Microbial Ecology, 69, 434–443. https://doi.org/10.1007/s00248-014-0554-7.
Amato, K. R., Sanders, J. G., Song, S. J., Nute, M., Metcalf, J. L., Thompson, L. R., Morton, J. T., Amir, A., McKenzie, V. J., Humphrey, G., Gogul, G., Gaffney, J., Baden, A. L., Britton, G. A. O., Cuozzo, F. P., Di Fiore, A., Dominy, N. J., Goldberg, T. A., Gomez, A., et al (2019). Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes. The ISME Journal, 13, 576–587. https://doi.org/10.1038/s41396-018-0175-0.
Andriambeloson, J.-B., Greene, L. K., & Blanco, M. B. (2020). Prolonged torpor in Goodman’s mouse lemur (Microcebus lehilahytsara) from the high-altitude orest of Tsinjoarivo, central-eastern Madagascar. Folia Primatologica, 91, 697–710. https://doi.org/10.1159/000509102.
Baniel, A., Amato, K. R., Beehner, J. C., Bergman, T. J., Mercer, A., Perlman, R. F., Petrullo, L., Reitsema, L., Sams, S., Lu, A., & Snyder-Mackler, N. (2021). Seasonal shifts in the gut microbiome indicate plastic responses to diet in wild geladas. Microbiome, 9, 1–20. https://doi.org/10.1186/s40168-020-00977-9.
Barelli, C., Albanese, D., Donati, C., Pindo, M., Dallago, C., Rovero, F., Cavalieri, D., Tuohy, K. M., Hauffe, H. C., & De Filippo, C. (2015). Habitat fragmentation is associated to gut microbiota diversity of an endangered primate: Implications for conservation. Scientific Reports, 5, 14862. https://doi.org/10.1038/srep14862.
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Satistical SocietyB (Methodological), 57, 289–300.
Biddle, A., Stewart, L., Blanchard, J., & Leschine, S. (2013). Untangling the genetic basis of fibrolytic specialization by Lachnospiraceae and Ruminococcaceae in diverse gut communities. Diversity, 5, 627–640. https://doi.org/10.3390/d5030627.
Blanco, M. B., Greene, L. K., Rasambainarivo, F., Toomey, E., Williams, R. C., Andrianandrasana, L., Larsen, P. A., & Yoder, A. D. (2020). Next-generation technologies applied to age-old challenges in Madagascar. Conservation Genetics, 21, 785–793. https://doi.org/10.1007/s10592-020-01296-0.
Bolyen, E., Rideout, J. R., Dillon, M. R., Bokulich, N. A., Abnet, C., Al-Ghalith, G. A., Alexander, H., Alm, E. J., Arumugam, M., Asnicar, F., Bai, Y., Bisanz, J. E., Bittinger, K., Brejnrod, A., Brislawn, C. J., Brown, C. T., Callahan, B. J., Caraballo-Rodríguez, M., Chase, J., et al (2019). QIIME 2: Reproducible, interactive, scalable, and extensible microbiome data science. Nature Biotechnology, 37, 852–857. https://doi.org/10.1038/s41587-019-0209-9.
Brown, A., Lynch, D., Bouevitch, A., & Doukhanine, E. (2018). OMNIgene®• GUT provides easy self-collection and stabilization of liquid fecal samples for microbiome profiling. DNA Genotek https://www.dnagenotek.com/us/pdf/PD-WP-00056.pdf. Downloaded on 1 May 2021.
Clayton, J. B., Gomez, A., Amato, K., Knights, D., Travis, D. A., Blekhman, R., Knight, R., Leigh, S., Stumpf, R., Wolf, T., Glander, K. E., Cabana, F., & Johnson, T. J. (2018). The gut microbiome of nonhuman primates: Lessons in ecology and evolution. American Journal of Primatology, 80, e22867. https://doi.org/10.1002/ajp.22867.
David, L. A., Maurice, C. F., Carmody, R. N., Gootenberg, D. B., Button, J. E., Wolfe, B. E., Ling, A. V., Devlin, A. S., Varma, Y., Fischbach, M. A., Biddinger, S. B., Dutton, R. J., & Turnbaugh, P. J. (2014). Diet rapidly and reproducibly alters the human gut microbiome. Nature, 505, 559–563. https://doi.org/10.1038/nature12820.
Dearing, M. D., & Kohl, K. D. (2017). Beyond fermentation: Other important services provided to gendothermic herbivores by their gut microbiota. Integrative and Comparative Biology, 57, 723–731. https://doi.org/10.1093/icb/icx020.
Delsuc, F., Metcalf, J. L., Wegener Parfrey, L., Song, S. J., González, A., & Knight, R. (2014). Convergence of gut microbiomes in myrmecophagous mammals. Molecular Ecology, 23, 1301–1317. https://doi.org/10.1111/mec.12501.
Dewar, R. E., & Richard, A. F. (2007). Evolution in the hypervariable environment of Madagascar. Proceedings of the National Academy of Sciences of the USA, 104, 13723–13727. https://doi.org/10.1073/pnas.0704346104.
Dewar, R. E., & Richard, A. F. (2012). Madagascar: A history of arrivals, what happened, and will happen next. Annual Review of Anthropology, 41, 495–517. https://doi.org/10.1146/annurev-anthro-092611-145758.
Dill-McFarland, K. A., Weimer, P. J., Pauli, J. N., Peery, M. Z., & Suen, G. (2015). Diet specialization selects for an unusal and simplified gut microbiota in two- and three-toed sloths. Environmental Microbiology, 18, 1391–1402.
Donati, G., Santini, L., Eppley, T. M., Arrigo-Nelson, S. J., Balestri, M., Boinski, S., Bollen, A., Bridgeman, L. L., Campera, M., Carrai, V., Chalise, M. K., Lewis, A. D., Hohmann, G., Kinnaird, M. F., Koenig, A., Kowalewski, M., Lahann, P., McLennan, M. R., Nekaris, A. K. I., et al (2017). Low levels of fruit nitrogen as drivers for the evolution of Madagascar’s primate communities. Scientific Reports, 7, 14406. https://doi.org/10.1038/s41598-017-13906-y.
Donohue, M. E., Asangba, A. E., Ralainirina, J., Weisrock, D. W., Stumpf, R. M., & Wright, P. C. (2019). Extensive variability in the gut microbiome of a highly-specialized and critically endangered lemur species across sites. American Journal of Primatology, 81, e23046. https://doi.org/10.1002/ajp.23046.
Dos Reis, M., Gunnell, G. F., Barba-Montoya, J., Wilkins, A., Yang, Z., & Yoder, A. D. (2018). Using phylogenomic data to explore the effects of relaxed clocks and calibration strategies on divergence time estimation: Primates as a test case. Systematic Biology, 67, 594–615. https://doi.org/10.0193/sysbio/syy001.
Douglas, G. M., Maffei, V. J., Zaneveld, J. R., Yurgel, S. N., Brown, J. R., Taylor, C. M., Huttenhower, C., & Langille, M. G. I. (2020). PICRUSt2 for prediction of metagenome functions. Natura Biotechnology, 38, 685–688. https://doi.org/10.1038/s41587-020-0548-6.
Flint, H. J., Scott, K. P., Duncan, S. H., Louis, P., & Forano, E. (2012). Microbial degradation of complex carbohydrates in the gut. Gut Microbes, 3, 289–306. https://doi.org/10.4161/gmic.19897.
Fu, X., Li, R., Zhang, T., Li, M., & Mou, H. (2019). Study on the ability of partially hydrolyzed guar gum to modulate the gut microbiota and relieve constipation. Journal of Food Biochemistry, 43, e12715. https://doi.org/10.1111/jfbc.12715.
Fu, X., Wei, X., Xiao, M., Han, Z., Secundo, F., & Mou, H. (2020). Properties of hydrolyzed guar gum fermented in vitro with pig fecal inocula and its favorable impacts on microbiota. Carbohydrate Polymers, 237, 116116. https://doi.org/10.1016/j.carbpol.2020.116116.
Ganzhorn, J. U. (1988). Food partitioning among Malagasy primates. Oecologia, 75, 436–450. https://doi.org/10.1007/BF00376949.
Gomez, A., Rothman, J. M., Petrzelkova, K., Yeoman, C. J., Vlckova, K., Umaña, J. D., Carr, M., Modry, D., Todd, A., Torralba, M., Nelson, K. E., Stumpf, R. M., Wilson, B. A., Blekhman, R., White, B. A., & Leigh, S. R. (2016). Temporal variation selects for diet–microbe co-metabolic traits in the gut of Gorilla spp. The ISME Journal, 10, 514–526. https://doi.org/10.1038/ismej.2015.146.
Greene, L. K., McKenney, E. A., O’Connell, T. M., & Drea, C. M. (2018). The critical role of dietary foliage in maintaining the gut microbiome and metabolome of folivorous sifakas. Scientific Reports, 8, 14482. https://doi.org/10.1038/s41598-018-32759-7.
Greene, L. K., Bornbusch, S. L., McKenney, E. A., Harris, R. L., Gorvetzian, S. R., Yoder, A. D., & Drea, C. M. (2019a). The importance of scale in comparative microbiome research: New insights from the gut and glands of captive and wild lemurs. American Journal of Primatology, 81, e22974. https://doi.org/10.1002/ajp.22974.
Greene, L. K., Clayton, J. B., Rothman, R. S., Semel, B. P., Semel, M. A., Gillespie, T. R., Wright, P. C., & Drea, C. M. (2019b). Local habitat, not phylogenetic relatedness, predicts gut microbiota better within folivorous than frugivorous lemur lineages. Biology Letters, 15, 20190028. https://doi.org/10.1098/rsbl.2019.0028.
Greene, L. K., Williams, C. V., Junge, R. E., Mahefarisoa, K. L., Rajaonarivelo, T., Rakotondrainibe, H., O'Connell, T. M., & Drea, C. M. (2020). A role for gut microbiota in host niche differentiation. The ISME Journal, 14, 1675–1687. https://doi.org/10.1038/s41396-020-0640-4.
Greene, L. K., Blanco, M. B., Rambeloson, E., Graubics, K., Fanelli, B., Colwell, R. R., & Drea, C. M. (2021). Gut microbiota of frugo-folivorous sifakas across environments. Animal Microbiome, 3, 39. https://doi.org/10.1186/s42523-021-00093-5.
Grond, K., Bell, K. C., Demboski, J. R., Santos, M., Sullivan, J. M., & Hird, S. M. (2020). No evidence for phylosymbiosis in western chipmunk species. FEMS Microbiology Ecology, 96, fiz182. https://doi.org/10.1093/femsec/fiz182.
Hicks, A. L., Lee, K. J., Couto-Rodriguez, M., Patel, J., Sinha, R., Guo, C., Olson, S. H., Seimon, A., Ondzie, A. U., Karesh, W. B., Reed, P., Cameron, K. N., Lipkin, W. I., & Williams, B. L. (2018). Gut microbiomes of wild great apes fluctuate seasonally in response to diet. Nature Communications, 9, 1–18. https://doi.org/10.1038/s41467-018-04204-w.
Hladik, C. M., & Charles-Dominique, P. (1974). The behaviour and ecology of the sportive lemur (Lepilemur mustelinus) in relation to its dietary peculiarities. In R. D. Martin, G. A. Doyle, & A. C. Walker (Eds.), Prosimian biology (pp. 23–37). Duckwork.
IUCN. (2021). The IUCN Red List of Threatened Species. Version 2021-1. https://www.iucnredlist.org. Downloaded on 17 August 2021.
Joly-Radko, M., & Zimmermann, E. (2010). Seasonality in gum and honeydew feeding in gray mouse lemurs. In A. M. Burrows & L. T. Nash (Eds.), The evolution of exudativory in primates (pp. 141–153). Springer. https://doi.org/10.1007/978-1-4419-6661-2.
Lambert, J. E., & Rothman, J. M. (2015). Fallback foods, optimal diets, and nutritional targets: primate responses to varying food availability and quality. Annual Review of Anthropology, 44, 493–512. https://doi.org/10.1146/annurev-anthro-102313-025928.
LeBlanc, J. G., Milani, C., de Giori, G. S., Sesma, F., van Sinderen, D., & Ventura, M. (2013). Bacteria as vitamin suppliers to their host: A gut microbiota perspective. Current Opinion in Biotechnology, 24, 160–168. https://doi.org/10.1016/j.copbio.2012.08.005.
Ley, R. E., Hamady, M., Lozupone, C., Turnbaugh, P. J., Ramey, R. R., Bircher, J. S., Schlegel, M. L., Tucker, T. A., Schrenzel, M. D., Knight, R., & Gordon, J. I. (2008). Evolution of mammals and their gut microbes. Science, 320, 1647–1651. https://doi.org/10.1126/science.1155725.
Lozupone, C., Lladser, M. E., Knights, D., Stombaugh, J., & Knight, R. (2011). UniFrac: An effective distance metric for microbial community comparison. The ISME Journal, 5, 169–172. https://doi.org/10.1038/ismej.2010.133.
Marciniak, S., Mughal, M. R., Godfrey, L. R., Bankoff, R. J., Randrianatoandro, H., Crowley, B. E., Bergey, C. M., Muldoon, K. M., Randrianasy, J., Raharivololona, B. M., Schuster, S. C., Malhi, R. S., Yoder, A. D., Louis Jr., E. E., Kistler, L., & Perry, G. H. (2021). Evolutionary and phylogenetic insights from a nuclear genome sequence of the extinct, giant,“subfossil” koala lemur Megaladapis edwardsi. Proceedings of the National Academy of Sciences of the USA, 118, e2022117118. https://doi.org/10.1073/pnas.2022117118.
Maruo, T., Sakamoto, M., Ito, C., Toda, T., & Benno, Y. (2008). Adlercreutzia equolifaciens gen. nov., sp. nov., an equol-producing bacterium isolated from human faeces, and emended description of the genus Eggerthella. International Journal of Systematic and Evolutionary Microbiology, 58, 1221–1227. https://doi.org/10.1099/ijs.0.65404-0
McKenney, E. A., Greene, L. K., Drea, C. M., & Yoder, A. D. (2017). Down for the count: Cryptosporidium infection depletes the gut microbiome in Coquerel’s sifakas. Microbial Ecology in Health and Disease, 28, 1335165. https://doi.org/10.1080/16512235.2017.1335165.
Moeller, A. H., Suzuki, T. A., Phifer-Rixey, M., & Nachman, M. W. (2018). Transmission modes of the mammalian gut microbiota. Science, 362, 453–457. https://doi.org/10.1126/science.aat7164.
Nishida, A. H., & Ochman, H. (2018). Rates of gut microbiome divergence in mammals. Molecular Ecology, 27, 1884–1897. https://doi.org/10.1111/mec.14473.
Nowak, K., & Lee, P. C. (2013). “Specialist” primates can be flexible in response to habitat alteration. In L. Marsh & C. Chapman (Eds.), Primates in fragments. Developments in Primatology: Progress and Prospects. Springer. https://doi.org/10.1007/978-1-4614-8839-2_14.
Oliphant, K., & Allen-Vercoe, E. (2019). Macronutrient metabolism by the human gut microbiome: Major fermentation by-products and their impact on host health. Microbiome, 7, 1–15. https://doi.org/10.1186/s40168-019-0704-8.
Onarman Umu, Ö. C., Fauske, A. K., Åkesson, C. P., Pérez de Nanclares, M., Sørby, R., Press, C. M., Øverland, M., & Sørum, H. (2018). Gut microbiota profiling in Norwegian weaner pigs reveals potentially beneficial effects of a high-fiber rapeseed diet. PLoS ONE, 13, e0209439. https://doi.org/10.1371/journal.pone.0209439.
Orkin, J. D., Campos, F. A., Myers, M. S., Hernandez, S. E. C., Guadamuz, A., & Melin, A. D. (2019). Seasonality of the gut microbiota of free-ranging white-faced capuchins in a tropical dry forest. The ISME Journal, 13, 183–196. https://doi.org/10.1038/s41396-018-0256-0.
Perofsky, A. C., Lewis, R. J., & Meyers, L. A. (2019). Terrestriality and bacterial transfer: A comparative study of gut microbiomes in sympatric Malagasy mammals. The ISME Journal, 13, 50–63. https://doi.org/10.1038/s41396-018-0251-5.
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., & Glöckner, F. O. (2012). The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research, 41, D590–D596. https://doi.org/10.1093/nar/gks1219.
R Core Team. (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria URL https://www.R-project.org/.
Radespiel, U., Ehresmann, P., & Zimmermann, E. (2003). Species-specific usage of sleeping sites in two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in northwestern Madagascar. American Journal of Primatology, 59, 139–151. https://doi.org/10.1002/ajp.10071.
Rojas, C. A., Ramirez-Barahona, S., Holekamp, K. E., & Theis, K. R. (2021). Host phylogeny and host ecology structure the mammalian gut microbiota at different taxonomic scales.. Animal Microbiome, 3, 33. https://doi.org/10.1101/2020.09.23.299727
RStudio Team. (2020). RStudio: Integrated development for R. RStudio, Inc. http://www.rstudio.com.
Sato, H., Ichino, S., & Hanya, G. (2014). Dietary modification by common brown lemurs (Eulemur fulvus) during seasonal drought conditions in western Madagascar. Primates, 55, 219–230. https://doi.org/10.1007/s10329-013-0392-0.
Sato, H., Santini, L., Patel, E. R., Campera, M., Yamashita, N., Colquhoun, I. C., & Donati, G. (2016). Dietary flexibility and feeding strategies of Eulemur: A comparison with Propithecus. International Journal of Primatology, 37, 109–129. https://doi.org/10.1007/s10764-015-9877-6.
Segata, N., Izard, J., Waldron, L., Gevers, D., Miropolsky, L., Garrett, W. S., & Huttenhower, C. (2011). Metagenomic biomarker discovery and explanation. Genome Biology, 12, R60. https://doi.org/10.1186/gb-2011-12-6-r60.
Singh, B., Mal, G., Sharma, D., Sharma, R., Antony, C. P., & Kalra, R. S. (2020). Gastrointestinal biotransformation of phytochemicals: Towards futuristic dietary therapeutics and functional foods. Trends in Food Science & Technology, 106, 64–77. https://doi.org/10.1016/j.tifs.2020.09.022.
Springer, A., Fichtel, C., Al-Ghalith, G. A., Koch, F., Amato, K. R., Clayton, J. B., Knights, D., & Kappeler, P. M. (2017). Patterns of seasonality and group membership characterize the gut microbiota in a longitudinal study of wild Verreaux's sifakas (Propithecus verreauxi). Ecology and Evolution, 7, 5732–5745. https://doi.org/10.1002/ece3.3148.
Thalmann, U. (2001). Food resource characteristics in two nocturnal lemurs with different social behavior: Avahi occidentalis and Lepilemur edwardsi. International Journal of Primatology, 22, 287–324. https://doi.org/10.1023/A:1005627732561.
Thorén, S., Quietzsch, F., Schwochow, D., Sehen, L., Meusel, C., Meares, K., & Radespiel, U. (2011). Seasonal changes in feeding ecology and activity patterns of two sympatric mouse lemur species, the gray mouse lemur (Microcebus murinus) and the golden-brown mouse lemur (M. ravelobensis), in northwestern Madagascar. International Journal of Primatology, 32, 566–586. https://doi.org/10.1007/s10764-010-9488-1.
Trosvik, P., Rueness, E. K., de Muinck, E. J., Moges, A., & Mekonnen, A. (2018). Ecological plasticity in the gastrointestinal microbiomes of Ethiopian Chlorocebus monkeys. Scientific Reports, 8, 20. https://doi.org/10.1038/s41598-017-18435-2.
Umanets, A., de Winter, I., IJdema, F., Ramiro-Garcia, J., van Hooft, P., Heitkönig, I. M., Prins, H. H. T., & Smidt, H. (2018). Occupancy strongly influences faecal microbial composition of wild lemurs. FEMS Microbiology Ecology, 94, fiy017. https://doi.org/10.1093/femsec/fiy017.
Wang, M., Wichienchot, S., He, X., Fu, X., Huang, Q., & Zhang, B. (2019). In vitro colonic fermentation of dietary fibers: Fermentation rate, short-chain fatty acid production and changes in microbiota. Trends in Food Science & Technology, 88, 1–9. https://doi.org/10.1016/j.tifs.2019.03.005.
Wong, J. M., De Souza, R., Kendall, C. W., Emam, A., & Jenkins, D. J. (2006). Colonic health: fermentation and short chain fatty acids. Journal of Clinical Gastroenterology, 40, 235–243. https://doi.org/10.1097/00004836-200603000-00015.
Wright, P. C. (1999). Lemur traits and Madagascar ecology: Coping with an island environment. American Journal of Physical Anthropology, 110, 31–72. https://doi.org/10.1002/(sici)1096-8644(1999)110:29+<31::aid-ajpa3>3.0.co;2-0.
Wyatt, G., Bayliss, C., & Holcroft, J. (1986). A change in human faecal flora in response to inclusion of gum arabic in the diet. British Journal of Nutrition, 55, 261–266. https://doi.org/10.1079/BJN19860033.
Zhan, J., Wu, C., Liu, M., Su, X., Zhan, K., & Zhao, G. (2017). Effects of alfalfa flavonoids as dietary additives on bacterial flora in the rumen of dairy cows. Acta Prataculturae Sinica, 26, 82–89. 10.11686/cyxb2016358
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We thank the managers, guides, and staff of the Anjajavy Lodge and Reserve for project facilitation, as well as the staff of MICET and the University of Antananarivo’s Mention Zoologie et Biodiversité Animale for help securing permits. We thank Dr. Bobby Schopler for his help sampling nocturnal lemurs. Sarah Owens and the Argonne National Laboratory provided timely sequencing data. Funding was provided by the NSF (BCS-1749898 to LKG and CMD); the Global Wildlife Conservation’s Lemur Conservation Action Fund and IUCN SOS (to MBB and LKG); the John Simon Guggenheim Foundation (to ADY), the Duke Lemur Center (to MBB and LKG); and Anjajavy le Lodge (to LKG, ER, HAR, and MBB). This is Duke Lemur Center publication #1488.
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LKG and MBB conceived of the study. LKG, ADY, CMD, and MBB acquired funding. LKG, ER, HAR, and MBB performed field work. LKG performed laboratory work under CMD. LKG and EDF completed bioinformatic and statistical analyses under ADY. LKG drafted the manuscript with help from MBB. All authors contributed to final manuscript preparation.
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Greene, L.K., Rambeloson, E., Rasoanaivo, H.A. et al. Gut Microbial Diversity and Ecological Specialization in Four Sympatric Lemur Species Under Lean Conditions. Int J Primatol 42, 961–979 (2021). https://doi.org/10.1007/s10764-021-00257-9
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DOI: https://doi.org/10.1007/s10764-021-00257-9