Skin bacterial microbiome diversity predicts lower activity levels in female, but not male, guppies, Poecilia reticulata

Abstract

While the link between the gut microbiome and host behaviour is well established, how the microbiomes of other organs correlate with behaviour remains unclear. Additionally, behaviour-microbiome correlations are likely sex-specific because of sex differences in behaviour and physiology, but this is rarely tested. Here, we tested whether the skin microbiome of the Trinidadian guppy, Poecilia reticulata, predicts fish activity level and shoaling tendency in a sex-specific manner. High-throughput sequencing revealed that the bacterial community richness on the skin (Faith's phylogenetic diversity) was correlated with both behaviours differently between males and females. Females with richer skin-associated bacterial communities spent less time actively swimming. Activity level was significantly correlated with community membership (unweighted UniFrac), with the relative abundances of 16 bacterial taxa significantly negatively correlated with activity level. We found no association between skin microbiome and behaviours among male fish. This sex-specific relationship between the skin microbiome and host behaviour may indicate sex-specific physiological interactions with the skin microbiome. More broadly, sex specificity in host-microbiome interactions could give insight into the forces shaping the microbiome and its role in the evolutionary ecology of the host.

Keywords: Trinidadian guppy; activity level; behaviour; sexual dimorphism; shoaling; skin microbiome.

Figure 1.

The diversity of the skin microbiome bacterial community (Faith's PD) did not significantly differ between male and female guppies (a), but bacterial community membership did (b) Principal coordinates plot of unweighted UniFrac distances between samples). Box plots give the median (dark line), interquartile range (box), values within 1.5 x the interquartile range (whiskers) and outliers (points).

Figure 2.

The proportion of time guppies spent swimming (a) and associating with a shoal (b) depended on an interaction between the diversity of the skin microbiome (Faith's PD) and host sex. Points are back-transformed partial residuals from the models, and curves and shading give the model fits and 95% confidence bands.