The Occasional Hymenoptera: Attine ants, fungus and antibiotics
Some 65-45 million years ago certain ants transitioned from the life of hunter-gatherers to that of farmer. The farmer ants (ants of the tribe Attini or attine ants) raise specific fungus for food. They take great care in the cultivation. Worker ants fertilize the fungus with manure brought from outside the nest, and a new queen will take a cultivar of the crop with her when forming a new nest.
The farming techniques of these ants have been studied for over a century. In that time there have been a number of theories to account for the origin of the fungus-growing behavior of the attine ants, all positing different substrates used by the ants to cultivate the fungus. In a review entitled “The origin of the attine ant-fungus mutualism,” 76 Q. Rev. Biol. 169 (2001) (abstract; full aarticle pdf) Ulrich G. Mueller (University of Texas), Cameron R. Currie (University of Wisconsin-Madison) and Ted R. Schultz (University of Maryland) concluded that mutualism between the ants and fungus probably arose either from interactions that the ants had with fungi that grew on the wall of nests built from leaf litter or from a system of fungal myrmecochory in which specialized fungi relied on ants for dispersal. Myrmecochory is a widespread mechanism adapted by certain plants to engage ants in their seed dispersal. Under the latter theory the ants acted as vectors for the fungus between the parent and offspring nests and eventually the mutualism between fungus and ant arose, with the ant cultivating the fungus.
Many insects eat fungi (springtails, beetles, flies, moths, termites and wood wasps) and some depend on fungus for a large portion of their diet. Certain macrotermites and wood-boring beetles also cultivate fungus for food. In ants, however, dependence on fungus as the principle food source has arisen only twice. Once in the attine ants (which is a monophyletic group consisting of 12 genera of over 200 species, all which cultivate fungus), and the other resulting in eight species of social parasites of the tribe Solenopsidini, which parasitize attine ants and eat the fungus cultivated by their hosts. Other ants have other symbiotic uses for fungus. Old World Lasius ants of the subgenera Dendrolasius and Chthonolasius, for example, nourish fungi with honeydew to bind shredded wood or soil into a composite building material. (Birgit C. Schlick-Steiner, et al.,”Specificity and transmission mosaic of ant nest-wall fungi,” 105 Proc. Nat’l Acad. Sciences 940 (2008) (full article)). In other ants fungi are beneficial endosymbionts in the gut. But the two instances of adaptions concerning cultivated fungus are the only known instances where ants use fungus as food.
Attine ants are confined to the New World and most live in the tropical parts of Mexico and Central and South America. In Africa and elsewhere this ecological niche is filled by termites. (This suggests that the ants arose after Gondwana separated South America from Africa.) According to Hölldobler and Wilson, The Ants (Springer-Verlag: 1990), p596, attine ants are unique among ants for having the following “unusual combination of anatomical traits”: “the shape of the antennal segments; a less-than-absolute tendency toward hard, spinose, or tuberulate bodies and a proportionately large, casement-like first gastral segment.”
Attine ants are separated into two groups. The “higher attines” include the five most derived genera (itself a monophyletic group), and the remaining seven genera compose the “lower attines” (a paraphyletic group by virtue of excluding the “higher attines”). All attine ants are fungus-growers, but two of the “higher attine” genera, Acromyrmex and Atta, go by the common name leaf-cutter ants. The lower attines typically use dead vegetative debris, insect feces and corpses as fertilizer; the “higher attines” usually use dead vegetable matter, except the leaf cutters which use mostly fresh leaves and flowers. Cameron R. Currie, “A Community of ants, fungi, and bacteria: A Multilateral Approach to Studying Symbiosis,” 55 Ann. Rev. Microbiology 357 (2001) (abstract; the full review article is behind a paywall).
The particular fungus cultivated was not precisely known until recently; the traditional methods of classifying fungi (by describing the morphology of fruiting structures) could not be used because the attine cultivars did not readily produce such structures. With the advent of molecular phylogenetic techniques it has been possible to show that the fungi are basidiomycetes, in the order Agaricales and in the tribe Leucocoprineae (see Currie (2001), above).
Now the fact that these Solenopsidini ants became parasites of the attine cultivars and given what we’ve already seen about parasites and parasitoids in other posts in this series, it would be surprising that the attine ants could cultivate this fungus without something arising that would feast on the food that the ants expend so much energy cultivating. As it turns out, the fungus is in fact subject to a specialized, virulent, and highly derived fungal pathogen, in the genus Escovopsis. To deal with this threat the ants have developed a mutualistic association with filamentous bacteria (actinomycetes) that produce antibiotics that suppress the growth of Escovopsis (see Currie (2001), above).
The ants have also developed a specialized division of labor to deal with possible contamination of the food supply. Specific roles were created to remove waste from the nest, since such waste is a source of pathogens which could contaminate the fungus. Adam G. Hart and Francis L.W. Ratnieks of the University of Sheffield have shown that the leaf cutter Atta colombica divide the workers that work outside the nest into two groups: those that collect leaves for fungus manure and those that deal with waste management. About 89% were foragers and 11% dealt with waste management. The groups were distinct; workers did not change tasks. The waste managers also had a division between those that transported the waste and those that tended to it. The foragers also avoided the dump sites even when this greatly extended their trails. “Waste management in the leaf-cutting ant Atta colombica,” 13 Behavioral Ecology 224 (2002) (abstract and free access).
With respect to the specific fungal pathogens Stephen J. Taerum (of University of Kansas) and others found by using molecular philogenetic techniques that on a finer level the relationship between Escovopsis and the specific species of leaf cutters (in the genera Acromyrmex and Atta) the host-pathogen relationship is not particularly specific. Thus the fungus-farming ants have to protect their crop from a wider range of pathogens than origially thought. “Low host–pathogen specificity in the leaf-cutting ant–microbe symbiosis,” 274 Proc. Royal Soc’y B 1971 (2007) (full access). The authors discuss the two leading theories of how the attine ants maintain antibiotic producing organisms.
This brings us to today’s story. Research led by Matthew I. Hutchings of the University of East Anglia seem to have discovered that attine ants use an antibiotic cocktail to combat the pathogens of their cultivated fungus. The paper is Joerg Barke, et al., “A mixed community of actinomycetes produce multiple antibiotics for the fungus farming ant Acromyrmex octospinosus,” published online by BMC Biology (provisional abstract and provision pdf open access).
The authors there discuss the two theories for the presence of antibiotic producing bacteria among the attine. One theory proposes that the bacteria from the genus Pseudonocardia are the sole, co-evolved mutualists of attine ants and are transmitted vertically by the queens. Recently a Pseudonocardia-produced antifungal, named dentigerumycin, associated with the lower attine Apterostigma dentigerum was discovered. This is consistent with the first theory. A second theory is that attine ants sample actinomycete bacteria from the soil, selecting and maintaining those species that make useful antibiotics. In this paper the authors describe how a Streptomyces species associated with “higher attine” Acromyrmex octospinosus was recently shown to produce the antifungal candicidin.The authors admit that the presence of the Steptomyces species in the nest could be an environmental contaminant. But it could also evidence the recruitment of useful actinomycetes by the ants from the environment.
In the press release by East Anglia Dr. Hutchings describes how the discovery of the new antibiotic-producing bacteria among the ants took place.