Host Bias in Diet-Source Microbiome Transmission in Wild Cohabitating Herbivores: New Knowledge for the Evolution of Herbivory and Plant Defense

Abstract

It is commonly understood that dietary nutrition will influence the composition and function of the animal gut microbiome. However, the transmission of organisms from the diet-source microbiome to the animal gut microbiome in the natural environment remains poorly understood, and elucidating this process may help in understanding the evolution of herbivores and plant defenses. Here, we investigated diet-source microbiome transmission across a range of herbivores (insects and mammals) living in both captive and wild environments. We discovered a host bias among cohabitating herbivores (leaf-eating insects and deer), where a significant portion of the herbivorous insect gut microbiome may originate from the diet, while in deer, only a tiny fraction of the gut microbiome is of dietary origin. We speculated that the putative difference in the oxygenation level in the host digestion systems would lead to these host biases in plant-source (diet) microbiome transmission due to the oxygenation living condition of the dietary plant's symbiotic microbiome. IMPORTANCE We discovered a host bias among cohabitating herbivores (leaf-eating insects and deer), where a significant portion of the herbivorous insect gut microbiome may originate from the diet, while in deer, only a tiny fraction of the gut microbiome is of dietary origin. We speculated that the putative difference in the oxygenation level in the host digestion systems would lead to these host biases in plant-source (diet) microbiome transmission due to the oxygenation living condition of the dietary plant's symbiotic microbiome. This study shed new light on the coevolution of herbivory and plant defense.

Keywords: diet-source microbiome transmission; gut microbiomes; host-plant interaction; wild herbivores.

FIG 1

The dominant microbial groups in diet and herbivores of this study. (A) Phylum level. (B) Genus level. Herbivorous insects included 43 pooled samples from the following: leaf-eating grasshoppers, locusts, and Pyralidae. Herbivorous mammals included 89 samples from the following: Père David’s Deer (milu), musk deer, and rabbits. Diet included 81 dietary plant samples and five forage samples. Cicadas were of the sap-sucking type.

FIG 2

The diet-source microbiome transmission in wild cohabitating herbivores. (A) ASVs (amplicon sequence variants) shared only between the gut microbiome herbivorous insects (leaf-eating grasshoppers and locusts) and dietary plants (left) and only between the gut microbiome of milu and dietary plants (right). (B) Mean proportion of diet-source microbiome in herbivorous insect gut microbiome (left) and milu gut microbiome (right). (C) Mean pairwise unweighted UniFrac distance between insect and diet samples (left) or between milu and diet samples (right). Nonparametric t test was used to test the significance of the difference. SAL, Spartina alterniflora; PAU, Phragmites australis; SGL, Suaeda glauca.

FIG 3

The putative phenotype in the microbiome in this study. (A) Proportion of putative aerobic. (B) Proportion of putative anaerobic. The Mann-Whitney-Wilcoxon test was used to assess the hypothesis of whether the proportion of aerobic microbiome in either insect gut microbiome or diet-source microbiome was significantly higher than that in the milu gut microbiome. Herbivorous insects included leaf-eating grasshoppers and locusts in the Dafeng region. Diet included dietary plants for the insects and milu in the Dafeng region.

FIG 4

The diet-source microbiome transmission across different herbivorous animals from invertebrates (wild Pyralidae insects and cicadas) to vertebrates (captive musk deer and rabbits). The first row presents the mean proportion of diet-source microbiome in herbivorous insect and mammal gut microbiome. The second row presents the mean pairwise unweighted UniFrac distance between herbivore and diet samples. Pyralidae collected in the Liyang region were adults. Pyralidae collected in the Anji region were adults and larva.