The topology and drivers of ant–symbiont networks across Europe

Abstract

Intimate associations between different species drive community composition across ecosystems. Understanding the ecological and evolutionary drivers of these symbiotic associations is challenging because their structure eventually determines stability and resilience of the entire species network. Here, we compiled a detailed database on naturally occurring ant–symbiont networks in Europe to identify factors that affect symbiont network topology. These networks host an unrivalled diversity of macrosymbiotic associations, spanning the entire mutualism–antagonism continuum, including: (i) myrmecophiles – commensalistic and parasitic arthropods; (ii) trophobionts – mutualistic aphids, scale insects, planthoppers and caterpillars; (iii) social parasites – parasitic ant species; (iv) parasitic helminths; and (v) parasitic fungi. We dissected network topology to investigate what determines host specificity, symbiont species richness, and the capacity of different symbiont types to switch hosts. We found 722 macrosymbionts (multicellular symbionts) associated with European ants. Symbiont type explained host specificity and the average relatedness of the host species. Social parasites were associated with few hosts that were phylogenetically highly related, whereas the other symbiont types interacted with a larger number of hosts across a wider taxonomic distribution. The hosts of trophobionts were the least phylogenetically related across all symbiont types. Colony size, host range and habitat type predicted total symbiont richness: ant hosts with larger colony size, a larger distribution range or with a wider habitat range contained more symbiont species. However, we found that different sets of host factors affected diversity in the different types of symbionts. Ecological factors, such as colony size, host range and niche width predominantly determined myrmecophile species richness, whereas host phylogeny was the most important predictor of mutualistic trophobiont, social parasite and parasitic helminth species richness. Lastly, we found that hosts with a common biogeographic history support a more similar community of symbionts. Phylogenetically related hosts also shared more trophobionts, social parasites and helminths, but not myrmecophiles. Taken together, these results suggest that ecological and evolutionary processes structure host specificity and symbiont richness in large‐scale ant–symbiont networks, but these drivers may shift in importance depending on the type of symbiosis. Our findings highlight the potential of well‐characterized bipartite networks composed of different types of symbioses to identify candidate processes driving community composition.

A remarkable legion of guests: Diversity and host specificity of army ant symbionts

“…Carl Rettenmeyer and colleagues listed about 50 insect guests of the army ant Eciton burchellii (Westwood, 1842) that have been collected either in and around army ants’ temporary nesting sites (bivouacs) or in colony emigrations (Rettenmeyer et al, 2011). This outstanding diversity might be explained by the area–diversity relationship of the theory of island biogeography (Darlington Jr, 1957; MacArthur & Wilson, 1967; Mittelbach, 2012)—a pervasive ecological pattern that is applicable to partially isolated ecosystems such as social insect colonies (Gotwald Jr, 1995; Hölldobler & Wilson, 1990; Kronauer & Pierce, 2011; Parmentier et al, 2020; Wilson, 1971). According to the theory (MacArthur & Wilson, 1967), large social insect colonies such as those of army ants are expected to harbour a high diversity of associated species, partly because of high microhabitat heterogeneity and low symbiont extinction rates (Gotwald Jr, 1995; Hölldobler & Wilson, 1990).…”

“…First attempts to acquire such information have been made by compiling host records across different collection sites (e.g., von Beeren & Tishechkin, 2017; Ivens et al, 2016; Kistner, 1979; Kistner & Jacobson, 1990; Rettenmeyer & Akre, 1966; Seevers & Dybas, 1943), which is a common approach to estimating a symbiont's host range (Glasier et al, 2018; Parmentier et al, 2020; Poulin & Morand, 2014). However, these composite lists suffer from several shortcomings (Poulin et al, 2011; Thompson, 2005).…”

Chemical and Behavioural Strategies along The Spectrum of Host Specificity in Ant-Associated Silverfish

“…A remarkable gradation of host speci city can be found in the different groups of arthropods associated with ants. Some species of these ant guests or myrmecophiles only target a single ant species or genus, whereas, at the other extreme, some may associate with all ant species in their distribution range [13]. In line with the positive association between host speci city in other symbiont systems [11,12], high host speci city in myrmecophiles is often linked with increased specialization in chemical ecology, behaviour and morphology [14][15][16][17].…”

Niche differences, not fitness differences, explain coexistence across ecological groups

“…We have focused on species pairs, which by definition contain few species and a single interaction type per pair. We can therefore not be sure that fitness di erences would continue to play a minor role for coexistence in communities with more species (Chu and Adler, 2015;Spaak and De Laender, 2021) inevitably hosting a more diverse set of species interaction types (Parmentier et al, 2020;Bartomeus et al, 2021), including asymmetric and higher-order interactions (Letten and Stou er, 2019;Levine, Bascompte, et al, 2017;Mayfield and Stou er, 2017). On the one hand, theory has shown that all else equal, species richness tends to not a ect niche di erences, while increasing fitness di erences (Spaak and De Laender, 2021).…”