Gut microbiome heritability is nearly universal but environmentally contingent

Laura Grieneisen; Mauna Dasari; Trevor J. Gould; Johannes R. Björk; Jean Christophe Grenier; Vania Yotova; David Jansen; Neil Gottel; Jacob B. Gordon; Niki H. Learn; Laurence R. Gesquiere; Tim L. Wango; Raphael S. Mututua; J. Kinyua Warutere; Long'ida Siodi; Jack A. Gilbert; Luis B. Barreiro; Susan C. Alberts; Jenny Tung; Elizabeth A. Archie; Ran Blekhman

doi:10.1126/science.aba5483

Gut microbiome heritability is nearly universal but environmentally contingent

Laura Grieneisen, Mauna Dasari, Trevor J. Gould, Johannes R. Björk, Jean Christophe Grenier, Vania Yotova, David Jansen, Neil Gottel, Jacob B. Gordon, Niki H. Learn, Laurence R. Gesquiere, Tim L. Wango, Raphael S. Mututua, J. Kinyua Warutere, Long'ida Siodi, Jack A. Gilbert, Luis B. Barreiro, Susan C. Alberts, Jenny Tung, Elizabeth A. ArchieRan Blekhman

Research output: Contribution to journal › Article › peer-review

86 Scopus citations

Abstract

Relatives have more similar gut microbiomes than nonrelatives, but the degree to which this similarity results from shared genotypes versus shared environments has been controversial. Here, we leveraged 16,234 gut microbiome profiles, collected over 14 years from 585 wild baboons, to reveal that host genetic effects on the gut microbiome are nearly universal. Controlling for diet, age, and socioecological variation, 97% of microbiome phenotypes were significantly heritable, including several reported as heritable in humans. Heritability was typically low (mean = 0.068) but was systematically greater in the dry season, with low diet diversity, and in older hosts. We show that longitudinal profiles and large sample sizes are crucial to quantifying microbiome heritability, and indicate scope for selection on microbiome characteristics as a host phenotype.

Original language	English (US)
Pages (from-to)	181-186
Number of pages	6
Journal	Science
Volume	373
Issue number	6551
DOIs	https://doi.org/10.1126/science.aba5483
State	Published - Jul 9 2021

Bibliographical note

Funding Information:
This work was directly supported by NSF DEB 1840223 (E.A.A., J.A.G.), NIH R21 AG055777 (E.A.A., R.B.), NIH R01 AG053330 (E.A.A.), and NIGMS R35 GM128716 (R.B.). We also acknowledge support from the University of Minnesota Grand Challenges in Biology Postdoctoral Fellowship (to L.G.), the Duke University Population Research Institute P2C-HD065563 (pilot award to J.T.), and Notre Dame’s Eck Institute for Global Health (E.A.A.) and Environmental Change Initiative (E.A.A.). Since 2000, ABRP has been supported by NSF and NIH, including IOS 1456832 (S.C.A.), IOS 1053461 (E.A.A.), DEB 1405308 (J.T.), IOS 0919200 (S.C.A.), DEB 0846286 (S.C.A.), DEB 0846532 (S.C.A.), IBN 0322781 (S.C.A.), IBN 0322613 (S.C.A.), BCS 0323553 (S.C.A.), BCS 0323596 (S.C.A.), P01AG031719 (S.C.A.), R21AG049936 (J.T., S.C.A.), R03AG045459 (J.T., S.C.A.), R01AG034513 (S.C.A.), R01HD088558 (J.T.), and P30AG024361 (S.C.A.). We also thank Princeton University, the Chicago Zoological Society, the Max Planck Institute for Demographic Research, the L.S.B. Leakey Foundation, and the National Geographic Society.

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Copyright © 2021 The Authors, some rights reserved.

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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. https://doi.org/10.1126/science.aba5483

Grieneisen, L, Dasari, M, Gould, TJ, Björk, JR, Grenier, JC, Yotova, V, Jansen, D, Gottel, N, Gordon, JB, Learn, NH, Gesquiere, LR, Wango, TL, Mututua, RS, Warutere, JK, Siodi, L, Gilbert, JA, Barreiro, LB, Alberts, SC, Tung, J, Archie, EA & Blekhman, R 2021, 'Gut microbiome heritability is nearly universal but environmentally contingent', Science, vol. 373, no. 6551, pp. 181-186. https://doi.org/10.1126/science.aba5483

@article{f9f03d9246b1434f87f286d8ab74f01a,

title = "Gut microbiome heritability is nearly universal but environmentally contingent",

abstract = "Relatives have more similar gut microbiomes than nonrelatives, but the degree to which this similarity results from shared genotypes versus shared environments has been controversial. Here, we leveraged 16,234 gut microbiome profiles, collected over 14 years from 585 wild baboons, to reveal that host genetic effects on the gut microbiome are nearly universal. Controlling for diet, age, and socioecological variation, 97% of microbiome phenotypes were significantly heritable, including several reported as heritable in humans. Heritability was typically low (mean = 0.068) but was systematically greater in the dry season, with low diet diversity, and in older hosts. We show that longitudinal profiles and large sample sizes are crucial to quantifying microbiome heritability, and indicate scope for selection on microbiome characteristics as a host phenotype.",

author = "Laura Grieneisen and Mauna Dasari and Gould, {Trevor J.} and Bj{\"o}rk, {Johannes R.} and Grenier, {Jean Christophe} and Vania Yotova and David Jansen and Neil Gottel and Gordon, {Jacob B.} and Learn, {Niki H.} and Gesquiere, {Laurence R.} and Wango, {Tim L.} and Mututua, {Raphael S.} and Warutere, {J. Kinyua} and Long'ida Siodi and Gilbert, {Jack A.} and Barreiro, {Luis B.} and Alberts, {Susan C.} and Jenny Tung and Archie, {Elizabeth A.} and Ran Blekhman",

note = "Funding Information: This work was directly supported by NSF DEB 1840223 (E.A.A., J.A.G.), NIH R21 AG055777 (E.A.A., R.B.), NIH R01 AG053330 (E.A.A.), and NIGMS R35 GM128716 (R.B.). We also acknowledge support from the University of Minnesota Grand Challenges in Biology Postdoctoral Fellowship (to L.G.), the Duke University Population Research Institute P2C-HD065563 (pilot award to J.T.), and Notre Dame{\textquoteright}s Eck Institute for Global Health (E.A.A.) and Environmental Change Initiative (E.A.A.). Since 2000, ABRP has been supported by NSF and NIH, including IOS 1456832 (S.C.A.), IOS 1053461 (E.A.A.), DEB 1405308 (J.T.), IOS 0919200 (S.C.A.), DEB 0846286 (S.C.A.), DEB 0846532 (S.C.A.), IBN 0322781 (S.C.A.), IBN 0322613 (S.C.A.), BCS 0323553 (S.C.A.), BCS 0323596 (S.C.A.), P01AG031719 (S.C.A.), R21AG049936 (J.T., S.C.A.), R03AG045459 (J.T., S.C.A.), R01AG034513 (S.C.A.), R01HD088558 (J.T.), and P30AG024361 (S.C.A.). We also thank Princeton University, the Chicago Zoological Society, the Max Planck Institute for Demographic Research, the L.S.B. Leakey Foundation, and the National Geographic Society. Publisher Copyright: Copyright {\textcopyright} 2021 The Authors, some rights reserved.",

year = "2021",

month = jul,

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doi = "10.1126/science.aba5483",

language = "English (US)",

volume = "373",

pages = "181--186",

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T1 - Gut microbiome heritability is nearly universal but environmentally contingent

AU - Grieneisen, Laura

AU - Dasari, Mauna

AU - Gould, Trevor J.

AU - Björk, Johannes R.

AU - Grenier, Jean Christophe

AU - Yotova, Vania

AU - Jansen, David

AU - Gottel, Neil

AU - Gordon, Jacob B.

AU - Learn, Niki H.

AU - Gesquiere, Laurence R.

AU - Wango, Tim L.

AU - Mututua, Raphael S.

AU - Warutere, J. Kinyua

AU - Siodi, Long'ida

AU - Gilbert, Jack A.

AU - Barreiro, Luis B.

AU - Alberts, Susan C.

AU - Tung, Jenny

AU - Archie, Elizabeth A.

AU - Blekhman, Ran

N1 - Funding Information: This work was directly supported by NSF DEB 1840223 (E.A.A., J.A.G.), NIH R21 AG055777 (E.A.A., R.B.), NIH R01 AG053330 (E.A.A.), and NIGMS R35 GM128716 (R.B.). We also acknowledge support from the University of Minnesota Grand Challenges in Biology Postdoctoral Fellowship (to L.G.), the Duke University Population Research Institute P2C-HD065563 (pilot award to J.T.), and Notre Dame’s Eck Institute for Global Health (E.A.A.) and Environmental Change Initiative (E.A.A.). Since 2000, ABRP has been supported by NSF and NIH, including IOS 1456832 (S.C.A.), IOS 1053461 (E.A.A.), DEB 1405308 (J.T.), IOS 0919200 (S.C.A.), DEB 0846286 (S.C.A.), DEB 0846532 (S.C.A.), IBN 0322781 (S.C.A.), IBN 0322613 (S.C.A.), BCS 0323553 (S.C.A.), BCS 0323596 (S.C.A.), P01AG031719 (S.C.A.), R21AG049936 (J.T., S.C.A.), R03AG045459 (J.T., S.C.A.), R01AG034513 (S.C.A.), R01HD088558 (J.T.), and P30AG024361 (S.C.A.). We also thank Princeton University, the Chicago Zoological Society, the Max Planck Institute for Demographic Research, the L.S.B. Leakey Foundation, and the National Geographic Society. Publisher Copyright: Copyright © 2021 The Authors, some rights reserved.

PY - 2021/7/9

Y1 - 2021/7/9

N2 - Relatives have more similar gut microbiomes than nonrelatives, but the degree to which this similarity results from shared genotypes versus shared environments has been controversial. Here, we leveraged 16,234 gut microbiome profiles, collected over 14 years from 585 wild baboons, to reveal that host genetic effects on the gut microbiome are nearly universal. Controlling for diet, age, and socioecological variation, 97% of microbiome phenotypes were significantly heritable, including several reported as heritable in humans. Heritability was typically low (mean = 0.068) but was systematically greater in the dry season, with low diet diversity, and in older hosts. We show that longitudinal profiles and large sample sizes are crucial to quantifying microbiome heritability, and indicate scope for selection on microbiome characteristics as a host phenotype.

AB - Relatives have more similar gut microbiomes than nonrelatives, but the degree to which this similarity results from shared genotypes versus shared environments has been controversial. Here, we leveraged 16,234 gut microbiome profiles, collected over 14 years from 585 wild baboons, to reveal that host genetic effects on the gut microbiome are nearly universal. Controlling for diet, age, and socioecological variation, 97% of microbiome phenotypes were significantly heritable, including several reported as heritable in humans. Heritability was typically low (mean = 0.068) but was systematically greater in the dry season, with low diet diversity, and in older hosts. We show that longitudinal profiles and large sample sizes are crucial to quantifying microbiome heritability, and indicate scope for selection on microbiome characteristics as a host phenotype.

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Gut microbiome heritability is nearly universal but environmentally contingent

Abstract

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