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

Data from: 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 ones 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 harboring 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, the ants’ microbiome is potentially 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

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

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

Caste-specific symbiont policing by workers of Acromyrmex fungus-growing ants

The interaction between leaf-cutting ants and their fungus garden mutualists is ideal for studying the evolutionary stability of interspecific cooperation. Although the mutualism has a long history of diffuse coevolution, there is ample potential for conflicts between the partners over the mixing and transmission of symbionts. Symbiont transmission is vertical by default, and both the ants and resident fungus actively protect the fungal monoculture growing in their nest against secondary introductions of genetically dissimilar symbionts from other colonies. An earlier study showed that mixtures of major and minor Acromyrmex workers eliminate alien fungus fragments even in subcolonies where their resident symbiont is not present. We hypothesize that the different tasks and behaviors performed by majors and minors are likely to select for differential responses to alien fungi. Major workers forage and cut new leaves and masticate them after delivery in the upper parts of the fungus garden and so are likely to more frequently encounter alien fungus than minor workers maintaining the established fungus garden and caring for the brood. We show that major workers of Acromyrmex echinatior indeed express stronger incompatibility reactions toward alien fungus garden fragments than minor workers. This implies that only the major workers, through recognition and exclusion of foreign fungus clones at their point of entry to the nest, have a realistic possibility to eliminate alien fungal tissue before it gets incorporated in the fungus garden and starts competing with the resident fungal symbiont. Copyright 2009, Oxford University Press.