Co-habiting ants and silverfish display a converging feeding ecology

Abstract

Background: Various 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 animals living with social hosts remains limited. 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 the Neoasterolepisma silverfish genus and a wider nicoletiid and lepismatid silverfish panel where divergent myrmecophilous lifestyles are observed.

Results: Stable isotope profiling (δ¹³C and δ¹⁵N) showed that the isotopic niches of granivorous Messor ants and Messor-specialized Neoasterolepisma exhibit a remarkable overlap within an ant nest. Trophic experiments and gut dissections further supported that these specialized Neoasterolepisma silverfish transitioned to a diet that includes plant seeds. In contrast, the isotopic niches of generalist Neoasterolepisma silverfish 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) of Weissella bacteria in Messor-specialized silverfish and the ant hosts.

Conclusions: Together, we show that social hosts are important determinants for the feeding ecology of symbiotic animals and can induce diet convergence.

Keywords: Weissella; Diet; Formicidae; Granivory; Microbiome; Myrmecophile; Stable isotopes; Symbiosis; Zygentoma.

Fig. 1

The average isotopic niche of different silverfish and ant species varies greatly within a single sampling locality. When multiple specimens of the same species were sampled within a nest, we calculated the average specific to that particular nest. Consequently, each data point represents the mean value of these nest-specific averages for the species (e.g. N. spectabile based on 12 nest averages of 53 individuals in total, see Table 1). Error bars correspond to standard errors (SE). Colours represent different lifestyles and sample types; dark green: Messor-specialized Neoasterolepisma (Additional file 3: Movie S2), light green: Aphaenogaster-specialized Neoasterolepisma (Additional file 4: Movie S3), dark blue: obligate generalist Neoasterolepisma (N. curtiseta, Additional file 5: Movie S4), and nicoletiid (P. pseudolepisma), light blue: facultative generalist L. baetica, light grey: unassociated, black: ant hosts, and orange: organic material of Messor nests. The mean values of ant-associated and unassociated L. baetica individuals are given separately. Silverfish belonging to the different lifestyle categories are illustrated in the right panel. Caption colour corresponds to the lifestyle

Fig. 2

The isotopic niche converges between host-specialized silverfish and ant hosts inhabiting the same nest. Different panels give the variation of δ¹³C and δ¹⁵N of silverfish species and their ant hosts across different nests. Each point represents the average ant worker (black or grey) or silverfish value (coloured) per nest: a Messor and Messor-specialized N. lusitanum, b Messor and Messor-specialized N. spectabile, c Aphaenogaster and Aphaenogaster-specialized N. delator, d obligate generalist nicoletiid P. pseudolepisma and Camponotus ants, e obligate generalist N. curtiseta and Camponotus and Aphaenogaster ants, f facultative generalist L. baetica and Tetramorium host. Error bars correspond to standard errors (SE). A grey band connects ant workers and silverfish from the same nest

Fig. 3

Myrmecophilous lifestyle shapes the silverfish microbiome. The Lepismatinae and Atelurinae phylogenies are depicted and are based on a 418-bp fragment of the mitochondrial COI gene. COI amplification was not successful for three silverfish samples and their symbiotic communities are depicted below their respective phylogenetic trees. Silverfish lifestyle is colour-coded (see right). Wolbachia infection is indicated by a black background within the row labelled with “w”. The unit for the microbiome density is the number of symbiotic rRNA copies per ng DNA. Leuconostocaceae is currently considered as a later synonym of Lactobacillaceae

Fig. 4

Ant nest determines the infection profile of Weissella bacteria in Messor-specialized silverfish. Ant and silverfish individuals are grouped according to nest origin. The relative abundances of heterofermentative Lactobacillaceae symbionts are visualized (see bottom). Silverfish lifestyle is colour-coded; dark green: Messor-specialized Neoasterolepisma, light green: Aphaenogaster-specialized, and blue: obligate generalist (N. curtiseta and A. formicaria). Plant seed material is indicated with an orange background. Silverfish species are identified by their abbreviated species name