Co-habiting ants and silverfish display a converging feeding ecology

Abstract

Species from a great number of animal taxa have specialized to living with social hosts. Depending on their level of specialization, these symbiotic animals are characterized by distinct behavioural, chemical, and morphological traits that enable close heterospecific interactions. Despite its functional importance, our understanding of the feeding ecology of specialized animals living with social hosts remains limited.In this study, we examined how host specialization of silverfish co-habiting with ants affects several components of their feeding ecology. We combined stable isotope profiling, feeding assays, phylogenetic reconstruction, and microbial community characterization of theNeoasterolepismasilverfish genus and a wider nicoletiid and lepismatid silverfish panel where divergent myrmecophilous lifestyles are observed.Stable isotope profiling (δ13C and δ15N) showed that the isotopic niches (proxy for trophic niches) of granivorousMessorants andMessor-specializedNeoasterolepismaexhibit a remarkable overlap within an ant nest. Trophic experiments and gut dissections further supported that these specializedNeoasterolepismasilverfish transitioned to a diet that includes plant seeds. In contrast, the isotopic niches of generalistNeoasterolepismasilverfish and generalist nicoletiid silverfish were clearly different from their ant hosts within the shared nest environment.The impact of the myrmecophilous lifestyle on feeding ecology was also evident in the internal silverfish microbiome. Compared to generalists,Messor-specialists exhibited a higher bacterial density and a higher proportion of heterofermentative lactic acid bacteria. Moreover, the nest environment explained the infection profile (or the 16S rRNA genotypes) ofWeissellabacteria inMessor-specialized silverfish and the ant hosts.Together, we show that social hosts are important determinants for the feeding ecology of symbiotic animals, and can induce diet convergence.