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^*

^*Korrespondierende/r Autor/-in für diese Arbeit

Klinik für Dermatologie, Allergologie und Venerologie

102 Zitate (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.

Originalsprache	Englisch
Aufsatznummer	6440
Zeitschrift	Nature Communications
Jahrgang	6
ISSN	1751-8628
DOIs	https://doi.org/10.1038/ncomms7440
Publikationsstatus	Veröffentlicht - 04.03.2015

Fördermittel

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.

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SDG 3 – Gesundheit und Wohlergehen

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Forschungsschwerpunkt: Infektion und Entzündung - Zentrum für Infektions- und Entzündungsforschung Lübeck (ZIEL)

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10.1038/ncomms7440

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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, Artikel 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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DO - 10.1038/ncomms7440

M3 - Journal articles

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SN - 1751-8628

VL - 6

JO - Nature Communications

JF - Nature Communications

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

Abstract

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