Selective enrichment of founding reproductive microbiomes allows extensive vertical transmission in a fungus-farming termite
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Selective enrichment of founding reproductive microbiomes allows extensive vertical transmission in a fungus-farming termite. / Sinotte, Veronica M.; Renelies-Hamilton, Justinn; Andreu-Sánchez, Sergio; Vasseur-Cognet, Mireille; Poulsen, Michael.
In: Proceedings of the Royal Society B: Biological Sciences, Vol. 290, No. 2009, 20231559, 2023.Research output: Contribution to journal › Journal article › Research › peer-review
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T1 - Selective enrichment of founding reproductive microbiomes allows extensive vertical transmission in a fungus-farming termite
AU - Sinotte, Veronica M.
AU - Renelies-Hamilton, Justinn
AU - Andreu-Sánchez, Sergio
AU - Vasseur-Cognet, Mireille
AU - Poulsen, Michael
PY - 2023
Y1 - 2023
N2 - Mutualistic coevolution can be mediated by vertical transmission of symbionts between host generations. Termites host complex gut bacterial communities with evolutionary histories indicative of mixed-mode transmission. Here, we document that vertical transmission of gut bacterial strains is congruent across parent to offspring colonies in four pedigrees of the fungus-farming termite Macrotermes natalensis. We show that 44% of the offspring colony microbiome, including more than 80 bacterial genera and pedigree-specific strains, are consistently inherited. We go on to demonstrate that this is achieved because colony-founding reproductives are selectively enriched with a set of non-random, environmentally sensitive and termite-specific gut microbes from their colonies of origin. These symbionts transfer to offspring colony workers with high fidelity, after which priority effects appear to influence the composition of the establishing microbiome. Termite reproductives thus secure transmission of complex communities of specific, co-evolved microbes that are critical to their offspring colonies. Extensive yet imperfect inheritance implies that the maturing colony benefits from acquiring environmental microbes to complement combinations of termite, fungus and vertically transmitted microbes; a mode of transmission that is emerging as a prevailing strategy for hosts to assemble complex adaptive microbiomes.
AB - Mutualistic coevolution can be mediated by vertical transmission of symbionts between host generations. Termites host complex gut bacterial communities with evolutionary histories indicative of mixed-mode transmission. Here, we document that vertical transmission of gut bacterial strains is congruent across parent to offspring colonies in four pedigrees of the fungus-farming termite Macrotermes natalensis. We show that 44% of the offspring colony microbiome, including more than 80 bacterial genera and pedigree-specific strains, are consistently inherited. We go on to demonstrate that this is achieved because colony-founding reproductives are selectively enriched with a set of non-random, environmentally sensitive and termite-specific gut microbes from their colonies of origin. These symbionts transfer to offspring colony workers with high fidelity, after which priority effects appear to influence the composition of the establishing microbiome. Termite reproductives thus secure transmission of complex communities of specific, co-evolved microbes that are critical to their offspring colonies. Extensive yet imperfect inheritance implies that the maturing colony benefits from acquiring environmental microbes to complement combinations of termite, fungus and vertically transmitted microbes; a mode of transmission that is emerging as a prevailing strategy for hosts to assemble complex adaptive microbiomes.
KW - coevolution
KW - Macrotermitinae
KW - microbiota
KW - social insects
KW - superorganism
KW - symbiosis
U2 - 10.1098/rspb.2023.1559
DO - 10.1098/rspb.2023.1559
M3 - Journal article
C2 - 37848067
AN - SCOPUS:85174750350
VL - 290
JO - Proceedings of the Royal Society B: Biological Sciences
JF - Proceedings of the Royal Society B: Biological Sciences
SN - 0962-8452
IS - 2009
M1 - 20231559
ER -
ID: 371464421