Ant–fungus mutualism

Ant–fungus mutualism is a symbiosis seen in certain ant and fungal species, in which ants actively cultivate fungus much like humans farm crops as a food source. In some species, the ants and fungi are dependent on each other for survival. The leafcutter ant is a well-known example of this symbiosis.[1] A mutualism with fungi is also noted in some species of termites in Africa.[2]

Atta colombica queen

Overview

Fungus-growing ants actively propagate, nurture and defend the basidiomycete cultivar.[3] In return, the fungus provides nutrients for the ants, which may accumulate in specialized hyphal-tips known as "gongylidia". In some advanced genera the queen ant may take a pellet of the fungus with her when she leaves to start a new colony.[4]

Types

There are five main types of agriculture that fungus-growing ants practice:[5] lower, coral fungi, yeast, generalized higher, and leafcutter agricultural systems. Lower agriculture is the most primitive system and is currently practiced by 80 species in 10 genera.[6][7] Coral-fungus agriculture is practiced by 34 species by a single derived clade within the genus Apterostigma.[7] The coral fungus farmers underwent a switch of cultivars between 10 and 20 million years ago to a non-leucocoprineacoeous fungus, which makes its choice of cultivar different from all other attines.[8][9] Yeast agriculture is practiced by 18 species of Cyphomyrmex rimosus. The C. rimosus group is hypothesized to have evolved growing fungus in a yeast form between 5 and 25 million years ago.[9] Generalized higher agriculture is practiced by 63 species in two genera and refers to the condition of highly domesticated fungus.[7] The fungi used in higher agriculture cannot survive without its agriculturalists to tend it and has phenotypic changes that allow for increased ease of ant harvesting.[9] Leafcutter agriculture, which is a more highly derived form of higher agriculture, is practiced by 40 species in two genera and has the most recent evolution, originating between 8 and 12 million years ago.[9] Leaf cutters use living biomass as the substrate to feed their fungi, whereas in all other types of agriculture, the fungus requires dead biomass.[9]

The attines

The ants of the Attini tribe (subfamily Myrmicinae) are obligatory fungicultivists. Attini form twelve genera with over 200 species, which for the most part cultivate Lepiotaceae fungi of the tribe Leucocoprineae.[2][3][10] These ants are typically subdivided into the "lower" and "higher" attines. One of the more distinguishing factors between these two subgroups is their respective cultivars and cultivar substrates. Lower attines have less specialized cultivars that more closely resemble Leucocoprineae found in the wild and use "ancestral substrates" composed of plant, wood, arthropod, and flower detritus. The higher attines, on the other hand, use freshly cut grass, leaves, and flowers as their fungi substrate (hence the common name "leafcutter ants") and cultivate highly derived fungi.[11] The cultivars of higher attines often have growths called gongylidia -—nutrient-rich structures that have evolved for easy harvesting, ingesting, and feeding to larvae, while simultaneously serving as propagules for the fungi.[2][12]

Secondary symbiotic relationships

There are additional symbiotic relationships that affect fungal agriculture. The fungus Escovopsis is a parasite in ant colonies, and the bacterium Pseudonocardia has a mutualistic relationship with ants. Pseudonocardia resides on the ants' integuments and assists in defending the ants from Escovopsis through the production of secondary metabolites.[13] In fact, some species of ants have evolved exocrine glands that apparently nourish the antibiotic-producing bacteria inside them.[14] A black yeast interferes with this mutualism. The yeast has a negative effect on the bacteria that normally produce antibiotics to kill the parasitic fungus and so may affect the ants' health by allowing the parasite to spread.[15]

Partner fidelity

Partner fidelity can be witnessed through vertical gene transmission of fungi when a new colony is begun.[16] First, the queen must mate with several males to inseminate her many eggs before she flies off to a different location to begin a new colony. As she leaves, she takes with her a cluster of mycelium (the vegetative portion of the fungus) and actually begins a new fungal garden at her resting point using this mycelium. This grows to become the new fungal farm complete with the genes of the original cultivar preserved for another generation of ants. The relationship between attine ants and the Lepiotaceae fungus is so specialized that in many cases the Lepiotaceae is not even found outside of ant colony nests. It is clear that evolutionary pressure has been exerted on these ants to develop such an organized system in which to feed the fungus and continue its reproduction.

Studies done (with the concept of the prisoner's dilemma in mind) to test what further drives partner fidelity among species have shown that external factors are an even greater driving force. The effects of cheating ants (ants who did not bring plant biomass for fungal food) had a much smaller effect on the fitness of the relationship than when the fungi cheated by not providing gongylidia. Both effects were exacerbated in the presence of infection by escovopsis, resulting in close to a 50% loss in fungal biomass.[17] It is clear that the risk of infection from parasites is a driving external factor in keeping these two species loyal to one another. Though external factors play a large role in maintaining fidelity between the mutualists, genetic evidence of vertical transmission of partner fidelity has been found among asexual, fungus cultivating ant species.[18] Factors such as vertical transmission do not play as strong a role as environmental factors in maintaining fidelity, as cultivar switching among ant species is not a highly uncommon practice.[16]

Evolution

Given the exclusive New World distribution of the over 200 fungus-growing ant species,[12] this mutualism is thought to have originated in the basin of the Amazon rainforest some 50–66 million years ago. This would be after the K-Pg event and before the Eocene Optimum. During the fallout of the K-Pg event, the ancestor of the attine ants speciated as the resources it depended on as a generalized hunter-gathered grew scarce. At the same time, the sister group of the attine ants Dacetina developed predatory behavior during the same drive for new resources [19]. The mutualism ant-fungus mutualism did not evolve symmetrically. Ants quickly lost the ability to synthesize arginine by losing the argininosuccinate lyase gene, the final step in the arginine biosynthesis pathway. This created an immediate dependency on their cultivars and is supported by the lack of reversal to hunter-gatherer lifestyles [20]. The species Cyatta abscondita is considered the most recent ancestor of all leaf-cutting ants.[21]

Though the ants are monophyletic, their symbionts are not. They fall roughly into three major groups, only G1 having evolved gongylidia. Some G2 species grow long hyphae that form a protective cover over the nest. Those in G3 are paraphyletic, the most heteregenous, and form the most loose relationships with their cultivators.[3] Studies now show that fungi belonging to lower attine ants are not obligate mutualists and are capable of free-living. The fungi were earlier thought to be propagated by ants purely through clonal (vegetative) means. However considerable genetic variation in the fungi suggests that this may not be the case.[22]

It is hypothesized that fungi have evolved to make themselves more attractive to ant species through the development of enzymes that allow the ants to access nutrition in the fungal mass.[23]. This most likely occurred 25-35 million years ago, when attine ants domesticated their fungal cultivars in dry or seasonally dry locations in Central or North America, allowing for genetic isolation of the fungus. This development is the transition from lower agriculture to higher agriculture. During this period the fungal cultivars lost a series of genes that allowed them to decompose a wide variation of substrates [24]. At the same time they appear to have committed fully to propagation by the vertical transmission practiced by attine ants and at the end of their allopatry were no longer able to sexually reproduce with their free-living cousins or lower-attine counterparts [25].

A further specialization occurred from the opportunity that this coevolution offered. Up until this point the ant host had been feeding their cultivars primarily with detritus and fecal matter [26]. The shift towards herbivory consisted of certain groups of attine ants (the ancestors of Atta and Acromyrmex) shifting towards fresh plant matter as a substrate for growing their gardens [27] [28]. This shift provided the opportunity for the development of industrial-scale agriculture that we now see in the Atta and Acromyrmex genera.

There is debate in the field on the "tightness" of the coevolution between ants and their fungal cultivars. While the observed vertical transmission of fungal cultivars[29] and strong host-symbiont specificity[6][22] might suggest a tight coevolutionary relationship, recent phylogenetic analyses suggest this is not the case. Multiple domestications of the same fungus, fungal escape from domestication, or cultivar switching could lead to the observed diffuse coevolutionary pattern.[30] The alternative perspective of a "tight" coevolution points to evidence of instability in horizontal transmission events,[31][32] while also postulating that the observed differences between the phylogenies of attine ants and their fungal cultivars correspond to speciation events.[33]

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See also

References
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