Bacterial communities within Phengaris (Maculinea) alcon caterpillars are shifted following transition from solitary living to social parasitism of Myrmica ant colonies

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.

First Insight into Microbiome Profiles of Myrmecophilous Beetles and Their Host, Red Wood Ant Formica polyctena (Hymenoptera: Formicidae)—A Case Study

“…We found that all tested bacterial communities were predominated by three phyla (Proteobacteria, Actinobacteria, and Firmicutes), with each comprising a different share of the microbiome depending on species or sample tested (Table S1). Those phyla are frequently listed as the most abundant in bacterial communities associated with insect taxa [61][62][63][64], including ants [49,[65][66][67][68][69][70] and myrmecophilous caterpillars of Lycaenidae butterflies [71][72][73]. In some cases, the joint abundance of those phyla may exceed even 90% of bacterial community membership [63].…”

Chemical, Physiological and Molecular Responses of Host Plants to Lepidopteran Egg-Laying

“…Symbiotic bacteria play a pivotal role in the development and survival of their insect hosts, providing a full array of molecules for digestion, detoxification, and defense against pathogens (Douglas, 2015). There is still a scant knowledge on Lepidoptera-associated microbiomes, because the majority of studies is (i) merely descriptive, (ii) focused on single bacterial taxon, (iii) a few butterfly/moth species have been extensively surveyed, or (iv) only rarely endosymbionts have been compared across different developmental instars (Di Salvo et al, 2019;Gao et al, 2019;Szenteczki et al, 2019). Nevertheless, an increasing number of experiments provide evidence for a crucial function of microbes in basic physiological processes of Lepidoptera (Paniagua Voirol et al, 2018), e.g.…”

The microbiota of the Lasius fuliginosus – Pella laticollis myrmecophilous interaction

“…In turn, Fischer et al (2017) have shown that bacteria may contribute to the recognition of distant aphid species by Lasius niger ants (Fischer et al 2017). These results strengthen interest in studying the role of microorganisms in shaping relationships among closely associated species (Szenteczki et al 2019;Kaczmarczyk-Ziemba et al 2020).…”

“…The microbiota of Lasius fuliginosus and Pella laticollis 2019; Szenteczki et al 2019;Kaczmarczyk-Ziemba et al 2020)). In the present study, we have extended the state of the art regarding the microbiota of ants and their associates by investigating the potential similarities among the bacterial communities associated with two closely interacting species, L. fuliginosus and P. laticollis (both larvae and adults).…”