Analysis of intestinal microbiota in hybrid house mice reveals evolutionary divergence in a vertebrate hologenome

Jun Wang; Shirin Kalyan; Natalie Steck; Leslie M. Turner; Bettina Harr; Sven Künzel; Marie Vallier; Robert Häsler; Andre Franke; Hans Heinrich Oberg; Saleh M. Ibrahim; Guntram A. Grassl; Dieter Kabelitz; John F. Baines

doi:10.1038/ncomms7440

Analysis of intestinal microbiota in hybrid house mice reveals evolutionary divergence in a vertebrate hologenome

Jun Wang, Shirin Kalyan, Natalie Steck, Leslie M. Turner, Bettina Harr, Sven Künzel, Marie Vallier, Robert Häsler, Andre Franke, Hans Heinrich Oberg, Saleh M. Ibrahim, Guntram A. Grassl, Dieter Kabelitz, John F. Baines^*

^*Corresponding author for this work

Clinic of Dermatology, Allergology and Venerology

102 Citations (Scopus)

Abstract

Recent evidence suggests that natural selection operating on hosts to maintain their microbiome contributes to the emergence of new species, that is, the 'hologenomic basis of speciation'. Here we analyse the gut microbiota of two house mice subspecies, Mus musculus musculus and M. m. domesticus, across their Central European hybrid zone, in addition to hybrids generated in the lab. Hybrid mice display widespread transgressive phenotypes (that is, exceed or fall short of parental values) in a variety of measures of bacterial community structure, which reveals the importance of stabilizing selection operating on the intestinal microbiome within species. Further genetic and immunological analyses reveal genetic incompatibilities, aberrant immune gene expression and increased intestinal pathology associated with altered community structure among hybrids. These results provide unique insight into the consequences of evolutionary divergence in a vertebrate 'hologenome', which may be an unrecognized contributing factor to reproductive isolation in this taxonomic group.

Original language	English
Article number	6440
Journal	Nature Communications
Volume	6
ISSN	1751-8628
DOIs	https://doi.org/10.1038/ncomms7440
Publication status	Published - 04.03.2015

Funding

We thank Silke Carstensen, Jan Schubert, Katja Cloppenborg-Schmidt, Dorina Ölsner and Tanja Wesse for excellent technical assistance; Kim Steige and Miriam Linnenbrink for assistance in the field; Christine Pfeifle and Pankaj Barua for assistance in mouse husbandry; and Arne Nolte and Fabian Staubach for helpful discussion. This work was supported by the Deutsche Forschungsgemeinschaft (DFG) Excellence Cluster 306 ‘Inflammation at Interfaces’ and the Max Planck Society.

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

Research Areas and Centers

Academic Focus: Center for Infection and Inflammation Research (ZIEL)

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10.1038/ncomms7440

Cite this

Wang, J., Kalyan, S., Steck, N., Turner, L. M., Harr, B., Künzel, S., Vallier, M., Häsler, R., Franke, A., Oberg, H. H., Ibrahim, S. M., Grassl, G. A., Kabelitz, D., & Baines, J. F. (2015). Analysis of intestinal microbiota in hybrid house mice reveals evolutionary divergence in a vertebrate hologenome. Nature Communications, 6, Article 6440. https://doi.org/10.1038/ncomms7440

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title = "Analysis of intestinal microbiota in hybrid house mice reveals evolutionary divergence in a vertebrate hologenome",

abstract = "Recent evidence suggests that natural selection operating on hosts to maintain their microbiome contributes to the emergence of new species, that is, the 'hologenomic basis of speciation'. Here we analyse the gut microbiota of two house mice subspecies, Mus musculus musculus and M. m. domesticus, across their Central European hybrid zone, in addition to hybrids generated in the lab. Hybrid mice display widespread transgressive phenotypes (that is, exceed or fall short of parental values) in a variety of measures of bacterial community structure, which reveals the importance of stabilizing selection operating on the intestinal microbiome within species. Further genetic and immunological analyses reveal genetic incompatibilities, aberrant immune gene expression and increased intestinal pathology associated with altered community structure among hybrids. These results provide unique insight into the consequences of evolutionary divergence in a vertebrate 'hologenome', which may be an unrecognized contributing factor to reproductive isolation in this taxonomic group.",

author = "Jun Wang and Shirin Kalyan and Natalie Steck and Turner, \{Leslie M.\} and Bettina Harr and Sven K{\"u}nzel and Marie Vallier and Robert H{\"a}sler and Andre Franke and Oberg, \{Hans Heinrich\} and Ibrahim, \{Saleh M.\} and Grassl, \{Guntram A.\} and Dieter Kabelitz and Baines, \{John F.\}",

note = "Funding Information: We thank Silke Carstensen, Jan Schubert, Katja Cloppenborg-Schmidt, Dorina {\"O}lsner and Tanja Wesse for excellent technical assistance; Kim Steige and Miriam Linnenbrink for assistance in the field; Christine Pfeifle and Pankaj Barua for assistance in mouse husbandry; and Arne Nolte and Fabian Staubach for helpful discussion. This work was supported by the Deutsche Forschungsgemeinschaft (DFG) Excellence Cluster 306 {\textquoteleft}Inflammation at Interfaces{\textquoteright} and the Max Planck Society.",

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doi = "10.1038/ncomms7440",

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AU - Wang, Jun

AU - Kalyan, Shirin

AU - Steck, Natalie

AU - Turner, Leslie M.

AU - Harr, Bettina

AU - Künzel, Sven

AU - Vallier, Marie

AU - Häsler, Robert

AU - Franke, Andre

AU - Oberg, Hans Heinrich

AU - Ibrahim, Saleh M.

AU - Grassl, Guntram A.

AU - Kabelitz, Dieter

AU - Baines, John F.

N1 - Funding Information: We thank Silke Carstensen, Jan Schubert, Katja Cloppenborg-Schmidt, Dorina Ölsner and Tanja Wesse for excellent technical assistance; Kim Steige and Miriam Linnenbrink for assistance in the field; Christine Pfeifle and Pankaj Barua for assistance in mouse husbandry; and Arne Nolte and Fabian Staubach for helpful discussion. This work was supported by the Deutsche Forschungsgemeinschaft (DFG) Excellence Cluster 306 ‘Inflammation at Interfaces’ and the Max Planck Society.

PY - 2015/3/4

Y1 - 2015/3/4

N2 - Recent evidence suggests that natural selection operating on hosts to maintain their microbiome contributes to the emergence of new species, that is, the 'hologenomic basis of speciation'. Here we analyse the gut microbiota of two house mice subspecies, Mus musculus musculus and M. m. domesticus, across their Central European hybrid zone, in addition to hybrids generated in the lab. Hybrid mice display widespread transgressive phenotypes (that is, exceed or fall short of parental values) in a variety of measures of bacterial community structure, which reveals the importance of stabilizing selection operating on the intestinal microbiome within species. Further genetic and immunological analyses reveal genetic incompatibilities, aberrant immune gene expression and increased intestinal pathology associated with altered community structure among hybrids. These results provide unique insight into the consequences of evolutionary divergence in a vertebrate 'hologenome', which may be an unrecognized contributing factor to reproductive isolation in this taxonomic group.

AB - Recent evidence suggests that natural selection operating on hosts to maintain their microbiome contributes to the emergence of new species, that is, the 'hologenomic basis of speciation'. Here we analyse the gut microbiota of two house mice subspecies, Mus musculus musculus and M. m. domesticus, across their Central European hybrid zone, in addition to hybrids generated in the lab. Hybrid mice display widespread transgressive phenotypes (that is, exceed or fall short of parental values) in a variety of measures of bacterial community structure, which reveals the importance of stabilizing selection operating on the intestinal microbiome within species. Further genetic and immunological analyses reveal genetic incompatibilities, aberrant immune gene expression and increased intestinal pathology associated with altered community structure among hybrids. These results provide unique insight into the consequences of evolutionary divergence in a vertebrate 'hologenome', which may be an unrecognized contributing factor to reproductive isolation in this taxonomic group.

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SN - 1751-8628

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JO - Nature Communications

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Analysis of intestinal microbiota in hybrid house mice reveals evolutionary divergence in a vertebrate hologenome

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