Abstract

Holobionts are defined as a host and its microbiota, however, only a fraction of the bacteria are inherited vertically and thus coevolve with the host. The “it’s the song, not the singer” theory proposes that functional traits, instead of taxonomical microbiota composition, could be preserved across generations if interspecies interaction patterns perpetuate themselves. We tested conservation of functional composition across generations using zooplankton, mosquito, and plant datasets. Then, we tested if there is a change of functional microbiota composition over time within a generation in human datasets. Finally, we simulated microbiota communities to investigate if (pairwise) interactions can lead to multiple stable community compositions. Our results suggest that the vertically transmitted microbiota starts a predictable change of functions performed by the microbiota over time, whose robustness depends on the arrival of diverse migrants. This succession culminates in a stable functional composition state. The results suggest that the host-microbiota interaction and higher order interactions in general have an important contribution to the robustness of the final community. If the proposed mechanism proves to be valid for a diverse array of host species, this would support the concept of holobionts being used as units of selection, including animal breeding, suggesting this has a wider applicability.

Highlights

  • Holobionts are defined as a host and its microbiota, only a fraction of the bacteria are inherited vertically and coevolve with the host

  • The mechanisms of symbiont microbiota inheritance and persistence vary across species of hosts and ­symbionts[6]. This phenomenon is observed throughout evolution, in the animal kingdom for instance, squid (Euprymna scolopes) parents release the bacteria Vibrio fischeri to open water and by that way transmitting the ­bacteria[7]; juvenile koalas get tannin degrading bacteria eating enriched maternal faeces called ‘pap’[8]; in chickens, bacteria from the cloaca and oviduct colonize the egg shell, egg white and from there, the ­embryo[9,10]; in livestock, new-borns are initially colonized through physical contact when passing through the birth c­ anal[4]; within the plant kingdom, some plants transmit specific bacteria and/or fungi via vegetative ­reproduction[11]

  • The main limitation of considering holobionts as units of selection is that it does it not directly account for the recurrence across generations of horizontally transmitted bacteria, which gave rise to the idea that the functions performed by the symbionts could self-perpetuate over host generations regardless of who is performing the function

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Summary

Introduction

Holobionts are defined as a host and its microbiota, only a fraction of the bacteria are inherited vertically and coevolve with the host. The mechanisms of symbiont microbiota inheritance and persistence vary across species of hosts and ­symbionts[6] This phenomenon is observed throughout evolution, in the animal kingdom for instance, squid (Euprymna scolopes) parents release the bacteria Vibrio fischeri to open water and by that way transmitting the ­bacteria[7]; juvenile koalas get tannin degrading bacteria eating enriched maternal faeces called ‘pap’[8]; in chickens, bacteria from the cloaca and oviduct colonize the egg shell, egg white and from there, the ­embryo[9,10]; in livestock, new-borns are initially colonized through physical contact when passing through the birth c­ anal[4]; within the plant kingdom, some plants transmit specific bacteria and/or fungi via vegetative ­reproduction[11]. The host regulates the Scientific Reports | (2021) 11:19007

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