Can social partnerships influence the microbiome? Insights from ant farmers and their trophobiont mutualists.

Mutualistic interactions with microbes have played a crucial role in the evolution and ecology of animal hosts. However, it is unclear what factors are most important in influencing particular host-microbe associations. While closely related animal species may have more similar microbiota than distantly related species due to phylogenetic contingencies, social partnerships with other organisms, such as those in which one animal farms another, may also influence an organism's symbiotic microbiome. We studied a mutualistic network of Brachymyrmex and Lasius ants farming several honeydew-producing Prociphilus aphids and Rhizoecus mealybugs to test whether the mutualistic microbiomes of these interacting insects are primarily correlated with their phylogeny or with their shared social partnerships. Our results confirm a phylogenetic signal in the microbiomes of aphid and mealybug trophobionts, with each species harbouring species-specific endosymbiont strains of Buchnera (aphids), Tremblaya and Sodalis (mealybugs), and Serratia (both mealybugs and aphids) despite being farmed by the same ants. This is likely explained by strict vertical transmission of trophobiont endosymbionts between generations. In contrast, our results show the ants' microbiome is possibly shaped by their social partnerships, with ants that farm the same trophobionts also sharing strains of sugar-processing Acetobacteraceae bacteria, known from other honeydew-feeding ants and which likely reside extracellularly in the ants' guts. These ant-microbe associations are arguably more "open" and subject to horizontal transmission or social transmission within ant colonies. These findings suggest that the role of social partnerships in shaping a host's symbiotic microbiome can be variable and is likely dependent on how the microbes are transmitted across generations.

Evolution of microbial markets.

Biological market theory has been used successfully to explain cooperative behavior in many animal species. Microbes also engage in cooperative behaviors, both with hosts and other microbes, that can be described in economic terms. However, a market approach is not traditionally used to analyze these interactions. Here, we extend the biological market framework to ask whether this theory is of use to evolutionary biologists studying microbes. We consider six economic strategies used by microbes to optimize their success in markets. We argue that an economic market framework is a useful tool to generate specific and interesting predictions about microbial interactions, including the evolution of partner discrimination, hoarding strategies, specialized versus diversified mutualistic services, and the role of spatial structures, such as flocks and consortia. There is untapped potential for studying the evolutionary dynamics of microbial systems. Market theory can help structure this potential by characterizing strategic investment of microbes across a diversity of conditions.

Studying the Complex Communities of Ants and Their Symbionts Using Ecological Network Analysis.

Ant colonies provide well-protected and resource-rich environments for a plethora of symbionts. Historically, most studies of ants and their symbionts have had a narrow taxonomic scope, often focusing on a single ant or symbiont species. Here we discuss the prospects of studying these assemblies in a community ecology context using the framework of ecological network analysis. We introduce three basic network metrics that we consider particularly relevant for improving our knowledge of ant-symbiont communities: interaction specificity, network modularity, and phylogenetic signal. We then discuss army ant symbionts as examples of large and primarily parasitic communities, and symbiotic sternorrhynchans as examples of generally smaller and primarily mutualistic communities in the context of these network analyses. We argue that this approach will provide new and complementary insights into the evolutionary and ecological dynamics between ants and their many associates, and will facilitate comparisons across different ant-symbiont assemblages as well as across different types of ecological networks.

Ants farm subterranean aphids mostly in single clone groups--an example of prudent husbandry for carbohydrates and proteins?

BACKGROUND: Mutualistic interactions are wide-spread but the mechanisms underlying their evolutionary stability and ecological dynamics remain poorly understood. Cultivation mutualisms in which hosts consume symbionts occur in phylogenetically diverse groups, but often have symbiont monocultures for each host. This is consistent with the prediction that symbionts should avoid coexistence with other strains so that host services continue to benefit relatives, but it is less clear whether hosts should always favor monocultures and what mechanisms they might have to manipulate symbiont diversity. Few mutualisms have been studied in sufficient genetic detail to address these issues, so we decided to characterize symbiont diversity in the complex mutualism between multiple root aphid species and Lasius flavus ants. After showing elsewhere that three of these aphid species have low dispersal and mostly if not exclusively asexual reproduction, we here investigate aphid diversity within and between ant nest mounds. RESULTS: The three focal species (Geoica utricularia, Forda marginata and Tetraneura ulmi) had considerable clonal diversity at the population level. Yet more than half of the ant mounds contained just a single aphid species, a significantly higher percentage than expected from a random distribution. Over 60% of these single-species mounds had a single aphid clone, and clones tended to persist across subsequent years. Whenever multiple species/clones co-occurred in the same mound, they were spatially separated with more than 95% of the aphid chambers containing individuals of a single clone. CONCLUSIONS: L. flavus "husbandry" is characterized by low aphid "livestock" diversity per colony, especially at the nest-chamber level, but it lacks the exclusive monocultures known from other cultivation mutualisms. The ants appear to eat most of the early instar aphids, so that adult aphids are unlikely to face limited phloem resources and scramble competition with other aphids. We suggest that such culling of carbohydrate-providing symbionts for protein ingestion may maintain maximal host yield per aphid while also benefitting the domesticated aphids as long as their clone-mates reproduce successfully. The cost-benefit logic of this type of polyculture husbandry has striking analogies with human farming practices based on slaughtering young animals for meat to maximize milk-production by a carefully regulated adult livestock population.

Aphid-farming ants.

Ivens and Kronauer provide an overview of the farming mutualism between ants and aphids, in which ants protect aphids in exchange for food.