Temporal patterns of gut microbiota in lemurs (Eulemur rubriventer) living in intact and disturbed habitats in a novel sample type.

desiccated samples gut microbiome longitudinal strepsirrhine

Journal

American journal of primatology
ISSN: 1098-2345
Titre abrégé: Am J Primatol
Pays: United States
ID NLM: 8108949

Informations de publication

Date de publication:
14 Jun 2024
Historique:
revised: 20 05 2024
received: 01 06 2023
accepted: 06 06 2024
medline: 14 6 2024
pubmed: 14 6 2024
entrez: 14 6 2024
Statut: aheadofprint

Résumé

The gut microbiome is a plastic phenotype; gut microbial composition is highly variable across an individual host's lifetime and between host social groups, and this variation has consequences for host health. However, we do not yet fully understand how longitudinal microbial dynamics and their social drivers may be influenced by ecological stressors, such as habitat degradation. Answering these questions is difficult in most wild animal systems, as it requires long-term collections of matched host, microbiome, and environmental trait data. To test if temporal and social influences on microbiome composition differ by the history of human disturbance, we leveraged banked, desiccated fecal samples collected over 5 months in 2004 from two ecologically distinct populations of wild, red-bellied lemurs (Eulemur rubriventer) that are part of a long-term study system. We found that social group explained more variation in microbiome composition than host population membership did, and that temporal variation in common microbial taxa was similar between populations, despite differences in history of human disturbance. Furthermore, we found that social group membership and collection month were both more important than individual lemur identity. Taken together, our results suggest that synchronized environments use can lead to synchronized microbial dynamics over time, even between habitats of varying quality, and that desiccated samples could become a viable approach for studying primate gut microbiota. Our work opens the door for other projects to utilize historic biological sample data sets to answer novel temporal microbiome questions in an ecological context.

Identifiants

pubmed: 38873762
doi: 10.1002/ajp.23656
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e23656

Subventions

Organisme : University of British Columbia
ID : ASPIRE GR024611
Organisme : National Science Foundation
ID : BCS-0424234
Organisme : Primate Conservation, Inc.
Organisme : Conservation International Primate Action Fund
Organisme : American Society of Primatologists
Organisme : University of Texas-Austin
Organisme : TPW Foundation

Informations de copyright

© 2024 The Author(s). American Journal of Primatology published by Wiley Periodicals LLC.

Références

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(12), 3537–3545.
Alberts, S. C., & Altmann, J. (2012). The Amboseli baboon research project: 40 years of continuity and change. In P. M. Kappeler, & D. P. Watts (Eds.), Long‐term field studies of primates (pp. 261–287). Springer Berlin Heidelberg.
Amato, K. R., Yeoman, C. J., Kent, A., Righini, N., Carbonero, F., Estrada, A., Rex Gaskins, H., Stumpf, R. M., Yildirim, S., Torralba, M., Gillis, M., Wilson, B. A., Nelson, K. E., White, B. A., & Leigh, S. R. (2013). Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. The ISME Journal, 7(7), 1344–1353.
Amir, A., McDonald, D., Navas‐Molina, J. A., Debelius, J., Morton, J. T., Hyde, E., Robbins‐Pianka, A., & Knight, R. (2017). Correcting for microbial blooms in fecal samples during room‐temperature shipping. mSystems, 2(2), 10–1128. https://doi.org/10.1128/mSystems.00199-16
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), 26.
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(1), 14862.
Bennett, G., Malone, M., Sauther, M. L., Cuozzo, F. P., White, B., Nelson, K. E., Stumpf, R. M., Knight, R., Leigh, S. R., & Amato, K. R. (2016). Host age, social group, and habitat type influence the gut microbiota of wild ring‐tailed lemurs (Lemur catta). American Journal of Primatology, 78(8), 883–892.
Björk, J. R., Dasari, M., Grieneisen, L., & Archie, E. A. (2019). Primate microbiomes over time: Longitudinal answers to standing questions in microbiome research. American Journal of Primatology, 81(10–11), e22970.
Björk, J. R., Dasari, M. R., Roche, K., Grieneisen, L., Gould, T. J., Grenier, J.‐C., Yotova, V., Gottel, N., Jansen, D., Gesquiere, L. R., Gordon, J. B., Learn, N. H., Wango, T. L., Mututua, R. S., Kinyua Warutere, J., Siodi, L. 'ida, Mukherjee, S., Barreiro, L. B., Alberts, S. C., & Archie, E. A. (2022). Synchrony and idiosyncrasy in the gut microbiome of wild baboons. Nature Ecology & Evolution, 6, 1–10.
Blekhman, R., Tang, K., Archie, E. A., Barreiro, L. B., Johnson, Z. P., Wilson, M. E., Kohn, J., Yuan, M. L., Gesquiere, L., Grieneisen, L. E., & Tung, J. (2016). Common methods for fecal sample storage in field studies yield consistent signatures of individual identity in microbiome sequencing data. Scientific Reports, 6, 31519.
Bokulich, N. A., Maldonado, J., Kang, D.‐W., Krajmalnik‐Brown, R., & Caporaso, J. G. (2019). Rapidly processed stool swabs approximate stool microbiota profiles. mSphere, 4(2), e00208‐19. https://doi.org/10.1128/mSphere.00208-19
Bornbusch, S. L., Greene, L. K., Rahobilalaina, S., Calkins, S., Rothman, R. S., Clarke, T. A., LaFleur, M., & Drea, C. M. (2022). Gut microbiota of ring‐tailed lemurs (Lemur catta) vary across natural and captive populations and correlate with environmental microbiota. Animal Microbiome, 4(1), 29.
Bradley, B. J., Boesch, C., & Vigilant, L. (2000). Identification and redesign of human microsatellite markers for genotyping wild chimpanzee (Pan troglodytes verus) and gorilla (gorilla) DNA from faeces. Conservation Genetics, 1(3), 289–292.
Brockman, D. K., Whitten, P. L., Richard, A. F., & Schneider, A. (1998). Reproduction in free‐ranging male Propithecus verreauxi: The hormonal correlates of mating and aggression. American Journal of Physical Anthropology, 105(2), 137–151.
Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A., & Holmes, S. P. (2016). DADA2: High‐resolution sample inference from illumina amplicon data. Nature Methods, 13(7), 581–583.
Chandrashekar, A., Knierim, J. A., Khan, S., Raboin, D. L., Venkatesh, S., Clarke, T. A., Cuozzo, F. P., LaFleur, M., Lawler, R. R., Parga, J. A., Rasamimanana, H. R., Reuter, K. E., Sauther, M. L., & Baden, A. L. (2020). Genetic population structure of endangered ring‐tailed lemurs (Lemur catta) from nine sites in Southern Madagascar. Ecology and Evolution, 10(15), 8030–8043.
Chapman, C. A., Corriveau, A., Schoof, V. A. M., Twinomugisha, D., & Valenta, K. (2017). Long‐term simian research sites: Significance for theory and conservation. Journal of Mammalogy, 98(3), 652–660.
Cox, L. A., Comuzzie, A. G., Havill, L. M., Karere, G. M., Spradling, K. D., Mahaney, M. C., Nathanielsz, P. W., Nicolella, D. P., Shade, R. E., Voruganti, S., & VandeBerg, J. L. (2013). Baboons as a model to study genetics and epigenetics of human disease. ILAR Journal, 54(2), 106–121.
Cusick, J. A., Wellman, C. L., & Demas, G. E. (2021). The call of the wild: Using non‐model systems to investigate microbiome‐behaviour relationships. Journal of Experimental Biology, 224(10), jeb224485. https://doi.org/10.1242/jeb.224485
Davidson, G. L., Raulo, A., & Knowles, S. (2020). Identifying microbiome‐mediated behaviour in wild vertebrates. Trends in Ecology & Evolution, 35(11), 972–980.
Davis, N. M., Proctor, D. M., Holmes, S. P., Relman, D. A., & Callahan, B. J. (2018). Simple statistical identification and removal of contaminant sequences in marker‐gene and metagenomics data. Microbiome, 6(1), 226.
Diakiw, L. O. (2017). Determinants of the adult microbiome: Kinship, dispersal, and social relationships (S. R. Tecot (ed.)). The University of Arizona. https://www.proquest.com/dissertations-theses/determinants-adult-microbiome-kinship-dispersal/docview/1908479475/se-2
Dinan, T. G., & Cryan, J. F. (2017). The microbiome‐gut‐brain axis in health and disease. Gastroenterology Clinics of North America, 46(1), 77–89.
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(10–11), e23046.
Durham, D. L. (2003). Variation in responses to forest disturbance and the risk of local extinction: A comparative study of wild Eulemurs at Ranomafana National Park, Madagascar (A. H. Harcourt (ed.)). University of California, Davis. https://www.proquest.com/dissertations-theses/variation-responses-forest-disturbance-risk-local/docview/305338798/se-2
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(2), 514–526.
Grieneisen, L., Blekhman, R., & Archie, E. (2023). How longitudinal data can contribute to our understanding of host genetic effects on the gut microbiome. Gut Microbes, 15(1), 2178797.
Grieneisen, L., Dasari, M., Gould, T. J., Björk, J. R., Grenier, J.‐C., Yotova, V., Jansen, D., Gottel, N., Gordon, J. B., Learn, N. H., Gesquiere, L. R., Wango, T. L., Mututua, R. S., Warutere, J. K., Siodi, L., Gilbert, J. A., Barreiro, L. B., Alberts, S. C., Tung, J., … Blekhman, R. (2021). Gut microbiome heritability is nearly universal but environmentally contingent. Science, 373(6551), 181–186.
Grieneisen, L. E., & Blekhman, R. (2018). Crowdsourcing our national gut. mSystems, 3(3), e00060‐18. https://doi.org/10.1128/mSystems.00060-18
Grieneisen, L. E., Charpentier, M. J. E., Alberts, S. C., Blekhman, R., Bradburd, G., Tung, J., & Archie, E. A. (2019). Genes, geology and germs: Gut microbiota across a primate hybrid zone are explained by site soil properties, not host species. Proceedings of the Royal Society B: Biological Sciences, 286(1901), 20190431.
Irwin, M., King, T., Ravoloharimanitra, M., Razafindramanana, J., & Tecot, S. (2021). Eulemur rubriventer (amended version of 2020 assessment). IUCN Red List of Threatened Species, 2021, e.T8203A189740044. https://www.iucnredlist.org/species/8203/189740044
Jacobs, R. L., & Bradley, B. J. (2016). Considering the influence of nonadaptive evolution on primate color vision. PLoS One, 11(3), e0149664.
Kolodny, O., & Schulenburg, H. (2020). Microbiome‐mediated plasticity directs host evolution along several distinct time scales. Philosophical Transactions of the Royal Society, B: Biological Sciences, 375(1808), 20190589.
Kolodny, O., Weinberg, M., Reshef, L., Harten, L., Hefetz, A., Gophna, U., Feldman, M. W., & Yovel, Y. (2019). Coordinated change at the colony level in fruit bat fur microbiomes through time. Nature Ecology & Evolution, 3(1), 116–124.
Kuznetsova, A., Brockhoff, P. B., & Christensen, R. H. B. (2017). lmerTest package: Tests in linear mixed effects models. Journal of Statistical Software, 82, 1–26.
Mallott, E. K., Borries, C., Koenig, A., Amato, K. R., & Lu, A. (2020). Reproductive hormones mediate changes in the gut microbiome during pregnancy and lactation in Phayre's leaf monkeys. Scientific Reports, 10(1), 9961.
Marotz, C., Cavagnero, K. J., Song, S. J., McDonald, D., Wandro, S., Humphrey, G., Bryant, M., Ackermann, G., Diaz, E., & Knight, R. (2021). Evaluation of the effect of storage methods on fecal, saliva, and skin microbiome composition. mSystems, 6(2). https://doi.org/10.1128/mSystems.01329-20
McCord, A. I., Chapman, C. A., Weny, G., Tumukunde, A., Hyeroba, D., Klotz, K., Koblings, A. S., Mbora, D. N. M., Cregger, M., White, B. A., Leigh, S. R., & Goldberg, T. L. (2013). Fecal microbiomes of non‐human primates in Western Uganda reveal species‐specific communities largely resistant to habitat perturbation. American Journal of Primatology, 76(4), 347–354.
McDonald, D., Hyde, E., Debelius, J. W., Morton, J. T., Gonzalez, A., Ackermann, G., Aksenov, A. A., Behsaz, B., Brennan, C., Chen, Y., DeRight Goldasich, L., Dorrestein, P. C., Dunn, R. R., Fahimipour, A. K., Gaffney, J., Gilbert, J. A., Gogul, G., Green, J. L., Hugenholtz, P., … Treuren, W. V. (2018). American gut: An open platform for citizen science microbiome research. mSystems, 3(3). https://doi.org/10.1128/mSystems.00031-18
McManus, N., Holmes, S. M., Louis, Jr. E. E., Johnson, S. E., Baden, A. L., & Amato, K. R. (2021). The gut microbiome as an indicator of habitat disturbance in a critically endangered lemur. BMC Ecology and Evolution, 21(1), 222.
Menke, S., Meier, M., & Sommer, S. (2015). Shifts in the gut microbiome observed in wildlife faecal samples exposed to natural weather conditions: lessons from time‐series analyses using next‐generation. Methods in Ecology and Evolution, 6, 1080–1087. https://doi.org/10.1111/2041-210X.12394
Merenlender, A. M. (1993). The effects of sociality on the demography and genetic structure of Lemur fulvus rufus (polygamous) and Lemur rubriventer (monogamous) and the conservation implications (A. Dobson (ed.)). University of Rochester. https://www.proquest.com/dissertations-theses/effects-sociality-on-demography-genetic-structure/docview/304052941/se-2
Murillo, T., Schneider, D., Fichtel, C., & Daniel, R. (2022). Dietary shifts and social interactions drive temporal fluctuations of the gut microbiome from wild redfronted lemurs. ISME Communications, 2(1), 1–11.
Murillo, T., Schneider, D., Heistermann, M., Daniel, R., & Fichtel, C. (2022). Assessing the drivers of gut microbiome composition in wild redfronted lemurs via longitudinal metacommunity analysis. Scientific Reports, 12(1), 21462.
Oksanen, J., Kindt, R., Legendre, P., O'Hara, B., Henry, M., Stevens, H., Oksanen, M. J., & Suggests, M. (2007). The vegan package. Community Ecology Package, 10(631–637), 719.
Orkin, J. D., Campos, F. A., Myers, M. S., Cheves Hernandez, S. E., 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(1), 183–196.
Overdorff, D. J. (1991). Ecological correlates to social structure in two prosimian primates: Eulemur fulvus rufous and Eulemur rubriventer in Madagascar (K. E. Glander (ed.)). Duke University. https://www.proquest.com/dissertations-theses/ecological-correlates-social-structure-two/docview/303953460/se-2
Overdorff, D. J., & Tecot, S. R. (2006). Social pair‐bonding and resource defense in wild red‐bellied lemurs (Eulemur rubriventer). In Lemurs: ecology and adaptation (pp. 235–254). Springer US.
Paulson, J. N., Pop, M., & Bravo, H. C. (2013). metagenomeSeq: Statistical analysis for sparse high‐throughput sequencing. Bioconductor Package, 1, 63.
Perofsky, A. C., Ancel Meyers, L., Abondano, L. A., Di Fiore, A., & Lewis, R. J. (2021). Social groups constrain the spatiotemporal dynamics of wild sifaka gut microbiomes. Molecular Ecology, 30(24), 6759–6775.
Petrullo, L., Ren, T., Wu, M., Boonstra, R., Palme, R., Boutin, S., McAdam, A. G., & Dantzer, B. (2022). Glucocorticoids coordinate changes in gut microbiome composition in wild North American red squirrels. Scientific Reports, 12(1), 2605.
Pribyl, A. L., Parks, D. H., Angel, N. Z., Boyd, J. A., Hasson, A. G., Fang, L., MacDonald, S. L., Wills, B. A., Wood, D. L. A., Krause, L., Tyson, G. W., & Hugenholtz, P. (2021). Critical evaluation of faecal microbiome preservation using metagenomic analysis. ISME Communications, 1(1), 1–10.
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., & Glöckner, F. O. (2013). The SILVA ribosomal RNA gene database project: Improved data processing and web‐based tools. Nucleic Acids Research, 41(Database issue), 590–596.
R Core Team. (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing.
Raulo, A., Ruokolainen, L., Lane, A., Amato, K., Knight, R., Leigh, S., Stumpf, R., White, B., Nelson, K. E., Baden, A. L., & Tecot, S. R. (2018). Social behaviour and gut microbiota in red‐bellied lemurs (Eulemur rubriventer): In search of the role of immunity in the evolution of sociality. Journal of Animal Ecology, 87(2), 388–399.
Ribas, M. P., García‐Ulloa, M., Espunyes, J., & Cabezón, O. (2023). Improving the assessment of ecosystem and wildlife health: Microbiome as an early indicator. Current Opinion in Biotechnology, 81, 102923.
Segata, N., Izard, J., Waldron, L., Gevers, D., Miropolsky, L., Garrett, W. S., & Huttenhower, C. (2011). Metagenomic biomarker discovery and explanation. Genome Biology, 12(6), R60.
Slevin, M. C., Houtz, J. L., & Bradshaw, 2nd D. J., Anderson, R. C. (2020). Evidence supporting the microbiota‐gut‐brain axis in a songbird. Biology Letters, 16(11), 20200430.
Song, S. J., Amir, A., Metcalf, J. L., Amato, K. R., Xu, Z. Z., Humphrey, G., & Knight, R. (2016). Preservation methods differ in fecal microbiome stability, affecting suitability for field studies. mSystems, 1(3). https://doi.org/10.1128/mSystems.00021-16
Stothart, M. R., Palme, R., & Newman, A. E. M. (2019). It's what's on the inside that counts: stress physiology and the bacterial microbiome of a wild urban mammal. Proceedings of the Royal Society B: Biological Sciences, 286(1913):20192111.
Tecot, S. R. (2008). Seasonality and predictability: The hormonal and behavioral responses of the red ‐bellied lemur, Eulemur rubriventer, in southeastern Madagascar (D. J. Overdorff (ed.)). The University of Texas at Austin. https://www.proquest.com/dissertations-theses/seasonality-predictability-hormonal-behavioral/docview/304814612/se-2
Tecot, S. R. (2013). Variable energetic strategies in disturbed and undisturbed rain forests: Eulemur rubriventer fecal cortisol levels in South‐Eastern Madagascar. In J. Masters, M. Gamba, & F. Génin (Eds.), Leaping ahead: Advances in prosimian biology (pp. 185–195). Springer.
Tecot, S. R., Irwin, M. T., & Raharison, J.‐L. (2019). Faecal glucocorticoid metabolite profiles in diademed sifakas increase during seasonal fruit scarcity with interactive effects of age/sex class and habitat degradation. Conservation Physiology, 7(1), coz001.
Tecot, S. R., Ossello, G. M., Smith, P. G., Rakotonirina, L. H. F., Telo, A., Rasendry N, V., Rakotonirina T, E., & Peñaherrera‐Aguirre, M. (2023). Diurnal fecal glucocorticoid metabolite rhythms in a cathemeral primate, the red‐bellied lemur (Eulemur rubriventer), and across mammalian species. American Journal of Primatology, 85(8), e23521.
Tetel, M. J., de Vries, G. J., Melcangi, R. C., Panzica, G., & O'Mahony, S. M. (2018). Steroids, stress and the gut microbiome‐brain axis. Journal of Neuroendocrinology, 30(2), e12548. https://doi.org/10.1111/jne.12548
Trevelline, B. K., Fontaine, S. S., Hartup, B. K., & Kohl, K. D. (2019). Conservation biology needs a microbial renaissance: A call for the consideration of host‐associated microbiota in wildlife management practices. Proceedings of the Royal Society B: Biological Sciences, 286(1895), 20182448.
Vlčková, K., Shutt‐Phillips, K., Heistermann, M., Pafčo, B., Petrželková, K. J., Todd, A., Modrý, D., Nelson, K. E., Wilson, B. A., Stumpf, R. M., White, B. A., Leigh, S. R., & Gomez, A. (2018). Impact of stress on the gut microbiome of free‐ranging Western lowland gorillas. Microbiology, 164(1), 40–44.
Wasimuddin, M.H., Malik, H., Ratovonamana, Y. R., Rakotondranary, S. J., Ganzhorn, J. U., & Sommer, S. (2022). Anthropogenic disturbance impacts gut microbiome homeostasis in a Malagasy primate. Frontiers in Microbiology, 13, 911275.
Wasser, S. K., Houston, C. S., Koehler, G. M., Cadd, G. G., & Fain, S. R. (1997). Techniques for application of faecal DNA methods to field studies of Ursids. Molecular Ecology, 6(11), 1091–1097.
Whitney, T. L., Mallot, E. M., Diakiw, L. O., Christie, D. M., Ting, N., Amato, K. R., Tecot, S., Baden, A.L. (accepted). Social and ecological factors shaping the gut microbiome of a pair‐living mammal in Madagascar. American Journal of Primatology.
Whitten, P. L., Brockman, D. K., & Stavisky, R. C. (1998). Recent advances in noninvasive techniques to monitor hormone‐behavior interactions. American Journal of Physical Anthropology, 107(Suppl. 27), 1–23.
Wright, P., King, S. J., Baden, A., & Jernvall, J. (2008). Aging in wild female lemurs: Sustained fertility with increased infant mortality. Interdisciplinary Topics in Gerontology, 36, 17–28.
Wright, P. C., Andriamihaja, B., Terborgh, J., Schaik, C.V., Davenport, L., & Madhu, R. (2002). Making a rain forest national park work in Madagascar: Ranomafana National Park and its long‐term research commitment. In Making parks work: Strategies for preserving tropical nature, (pp 112–136). Island Press.
Wright, P.C., Razafindratsita, V.R., & Jernvall, J. (2005). The key to Madagascar frugivores. In J. L. Dew, & J. P. Boubli (Eds.), Tropical fruits and frugivores: The search for strong interactors (pp. 121–138). Springer.
Ziegler, T. E., & Wittwer, D. J. (2005). Fecal steroid research in the field and laboratory: improved methods for storage, transport, processing, and analysis. American Journal of Primatology, 67(1), 159–174.

Auteurs

Laura Grieneisen (L)

Department of Biology, University of British Columbia-Okanagan Campus, Kelowna, BC, Canada.

Allison Hays (A)

Laboratory for the Evolutionary Endocrinology of Primates, University of Arizona, Tucson, AZ, USA.
School of Anthropology, University of Arizona, Tucson, AZ, USA.

Erica Cook (E)

Laboratory for the Evolutionary Endocrinology of Primates, University of Arizona, Tucson, AZ, USA.

Ran Blekhman (R)

Section of Genetic Medicine, Department of Medicine, University of Chicago, Chicago, IL, USA.

Stacey Tecot (S)

Laboratory for the Evolutionary Endocrinology of Primates, University of Arizona, Tucson, AZ, USA.
School of Anthropology, University of Arizona, Tucson, AZ, USA.

Classifications MeSH