Antibiotic-altered gut microbiota explain host memory plasticity and disrupt pace-of-life covariation for an aquatic snail

Abstract

There is mounting evidence that intestinal microbiota communities and their genes (the gut microbiome) influence how animals behave and interact with their environment, driving individual variation. Individual covariation in behavioural, physiological, and cognitive traits among individuals along a fast-slow continuum is thought to arise because these traits are linked as part of an adaptive pace-of-life strategy. Yet paradoxically, trait intercorrelation is absent or disrupted in some populations but not others. Here, we provide experimental evidence from aquatic pond snails (Lymnaea stagnalis) that environmental stressors and the gut microbiota explain host phenotypic plasticity and disrupted covariation among traits. Antibiotic exposure at varying levels of ecologically relevant concentrations had multiple effects starting with gut microbiota diversity, differential abundance, and inferred function. Memory declined in line with antibiotic concentrations that caused the most profound gut microbiota disruption, and although pace-of-life traits remained rigid, their covariation did not. Moreover, inferred microbial metabolic pathways with biologically relevant host functions explained individual and treatment variation in phenotypes. Together, our results point to the gut microbiome as a proximate mechanism influencing the emergence and maintenance of phenotypic variation within populations and highlights the need to decipher whether the gut microbiome's sensitivity to environmental pollution facilitates adaptive or maladaptive phenotypic plasticity.

Keywords: Lymnaea stagnalis; antibiotic pollution; behavioural plasticity; cognition; gut microbiota; memory; microbiome–gut–brain axis; pace-of-life; personality; syndromes.

Figure 1

Gut microbiota metrics according to antibiotic treatment for (A) differentially abundant OTUs described at the family level or to the nearest classified level; (B) beta diversity calculated as Aitchinson’s distance; (C) Shannon index; and (D) observed species and (E) Chao1 diversity. Coloured dots represent individual samples; black dots represent mean and lines standard error. Statistics are detailed in Supplementary Table 1 (OTUs), Supplementary Table 2 (beta diversity), and Supplementary Table 4 (Shannon index, observed, and Chao1 diversity).

Figure 2

Correlations between phenotypic traits as individual-coloured dots and regression lines (left panel) and Pearson’s correlation coefficient across 2000 bootstrap iterations. (A) Thigmotaxis and memory, (B) thigmotaxis and speed, (C) speed and memory, (D) metabolic rate and memory, (E) metabolic rate and thigmotaxis, and (F) metabolic rate and speed. ^*indicates correlated phenotypes where P < .05 and 95% CI do not overlap zero. † indicates correlated phenotypes where P < .1 and CI do not overlap zero. ▪ indicates correlated phenotypes where P < .1 and CI overlaps zero. Statistics are presented in Supplementary Table 5.

Figure 3

Effects of antibiotics on four phenotypes for (A) memory, (B) thigmotaxis, (C) speed, and (D) metabolic rate. Coloured dots represent individual samples; black dots represent mean and lines standard error. Statistics are presented in Supplementary Table 6.

Figure 4

Differentially abundant gut microbiota features across phenotypic traits and antibiotic exposure. (A) Differentially abundant OTUs described at the family level. (B) Significantly differentially abundant KO pathways for memory and whether these KOs were or were not differentially abundant in pace-of-life traits (thigmotaxis, speed, and metabolic rate) and antibiotic treatments. (C) KO pathways that predict at least two pace-of-life traits and whether these KOs were perturbed by the antibiotic treatments. Coef indicates statistical correlation coefficient from MaASLin2 output. ^*represents P < .05, ^ P < .01. P values are Benjamini–Hochberg-corrected for multiple comparisons. Full statistical outputs are presented in Supplementary Tables 7, 10, 11, and 14.