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, 9 (8), 4452-4464
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Bacterial Communities Within Phengaris (Maculinea) alcon Caterpillars Are Shifted Following Transition From Solitary Living to Social Parasitism of Myrmica Ant Colonies

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Bacterial Communities Within Phengaris (Maculinea) alcon Caterpillars Are Shifted Following Transition From Solitary Living to Social Parasitism of Myrmica Ant Colonies

Mark A Szenteczki et al. Ecol Evol.

Abstract

Bacterial symbionts are known to facilitate a wide range of physiological processes and ecological interactions for their hosts. In spite of this, caterpillars with highly diverse life histories appear to lack resident microbiota. Gut physiology, endogenous digestive enzymes, and limited social interactions may contribute to this pattern, but the consequences of shifts in social activity and diet on caterpillar microbiota are largely unknown. Phengaris alcon caterpillars undergo particularly dramatic social and dietary shifts when they parasitize Myrmica ant colonies, rapidly transitioning from solitary herbivory to ant tending (i.e., receiving protein-rich regurgitations through trophallaxis). This unique life history provides a model for studying interactions between social living, diet, and caterpillar microbiota. Here, we characterized and compared bacterial communities within P. alcon caterpillars before and after their association with ants, using 16S rRNA amplicon sequencing and quantitative PCR. After being adopted by ants, bacterial communities within P. alcon caterpillars shifted substantially, with a significant increase in alpha diversity and greater consistency in bacterial community composition in terms of beta dissimilarity. We also characterized the bacterial communities within their host ants (Myrmica schencki), food plant (Gentiana cruciata), and soil from ant nest chambers. These data indicated that the aforementioned patterns were influenced by bacteria derived from caterpillars' surrounding environments, rather than through transfers from ants. Thus, while bacterial communities are substantially reorganized over the life cycle of P. alcon caterpillars, it appears that they do not rely on transfers of bacteria from host ants to complete their development.

Keywords: 16S amplicon sequencing; Lepidoptera; Lycaenidae; Spiroplasma; butterflies; myrmecophily.

Conflict of interest statement

None declared.

Figures

Figure 1
Figure 1
Bacterial community composition within Phengaris alcon caterpillars and Myrmica schencki workers and larvae. There is a clear shift in community composition following P. alcon caterpillars’ transition to parasitizing M. schencki colonies. We observed notable decreases in the abundances of Pseudomonadaceae and Enterobacteriaceae and an increase in Actinomycetales following caterpillars’ transition to living inside ant colonies. Note: average relative abundances for each group, across the top 40 OTUs in terms of total read count (62.9% of the total dataset) are shown above
Figure 2
Figure 2
Multivariate representations of bacterial community composition (beta diversity), using nonmetric multidimensional scaling (NMDS) of Bray–Curtis dissimilarity (left) and principal coordinate analysis (PCoA) of unweighted UniFrac phylogenetic distances (right). Phengaris alcon caterpillars living in ant colonies (n = 9) appear to host more similar bacterial communities than caterpillars on plants (n = 13), in terms of beta dissimilarity. Note: both distance matrices were calculated from the Greengenes‐annotated dataset, with read counts rarefied to even sampling depth
Figure 3
Figure 3
Heatmap of the 40 most abundant OTUs, with Bray–Curtis clustering of sample types (X‐axis; groups collapsed by averaging OTU abundances) and OTUs (Y‐axis). Environmental and/or pathogenic bacteria appear to account for most of the differentiation between Phengaris alcon caterpillars on plants and caterpillars in ant colonies. However, Spiroplasma species also appear to be useful in distinguishing between groups. Note: OTUs with >97% identity were denoted with subscripts (i.e., 1a/1b), while those with <97% identity were separately numbered.
Figure 4
Figure 4
Boxplots representing total 16S rRNA gene copies per microlitre of DNA extraction in Phengaris alcon and Myrmica schencki samples. P. alcon caterpillars living inside ant colonies hosted more consistent, but not significantly different (Wilcoxon p > 0.05) total quantities of bacteria compared to P. alcon on plants. Note: two caterpillars living on plants from Switzerland, and all four caterpillars on plants from Spain are not shown above, as an insufficient quantity of DNA remained following 16S rRNA amplicon sequencing library preparation. Ant workers and larvae from the same nest were also (separately) pooled prior to extraction.

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