Ant–fungus mutualism

Atta colombica queen

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]

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 designed 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 and other. 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. The species Cyatta abscondita is considered the most recent ancestor of all leaf-cutting ants.[19]

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 the fungi themselves may not be completely dependent on the ants. 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.[20] 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.[21]

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[22] and strong host-symbiont specificity[6][20] 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.[23] The alternative perspective of a "tight" coevolution points to evidence of instability in horizontal transmission events,[24][25] while also postulating that the observed differences between the phylogenies of attine ants and their fungal cultivars correspond to speciation events.[26]

References

  1. ↑ B. Hölldobler; E.O. Wilson (1990). The Ants. Cambridge MA: Belknap. ISBN 0-674-48525-4.
  2. 1 2 3 Mueller, U. G.; Gerardo, N. M.; Aanen, D. K.; Six, D. L.; Schultz, T. R. (2005). "The Evolution of Agriculture in Insects". Annual Review of Ecology, Evolution, and Systematics. 36: 563–595. doi:10.1146/annurev.ecolsys.36.102003.152626.
  3. 1 2 3 I.H. Chapela; S.A. Rehner; T.R. Schultz; U.G. Mueller (9 Dec 1994). "Evolutionary history of the symbiosis between fungus-growing ants and their fungi". Science. 266 (5191): 1691–1694. Bibcode:1994Sci...266.1691C. PMID 17775630. doi:10.1126/science.266.5191.1691.
  4. ↑ N. Weber (1966). "Fungus-growing Ants". Science. 153 (3736): 584. Bibcode:1966Sci...153..587W. doi:10.1126/science.153.3736.587.
  5. ↑ Mehdiabadi, N. J.; T. R. Schultz (2009). "Natural history and phylogeny of the fungus-farming ants (Hymenoptera: Formicidae: Myrmicinae: Attini)". Myrmecological News. 13: 37–55.
  6. 1 2 Schultz, T. R.; S. G. Brady (2008). "Major evolutionary transitions in ant agriculture". Proceedings of the National Academy of Sciences of the United States of America. 105 (14): 5435–5440. Bibcode:2008PNAS..105.5435S. PMC 2291119 Freely accessible. PMID 18362345. doi:10.1073/pnas.0711024105.
  7. 1 2 3 Mehdiabdi and Schultz 2009
  8. ↑ Villesen, P., U. G. Mueller, T. R. Schultz, R. M. M. Adams, A. C. Bourck (2004). "Evolution of ant-cultivar specialization and cultivar switching in Apterostigma fungus-growing ants". Evolution. 58 (10): 2252–2265. PMID 15562688. doi:10.1554/03-203.
  9. 1 2 3 4 5 Schultz and Brady 2008
  10. ↑ Weber N. A. 1972. Gardening ants: The attines. Philadelphia (PA): American Philosophical Society.
  11. ↑ Schultz, T. R.; Meier, R. (1995). "A phylogenetic analysis of the fungus-growing ants (Hymenoptera: Formicidae: Attini) based on morphological characters of the larvae". Systematic Entomology. 20: 337–370. doi:10.1111/j.1365-3113.1995.tb00100.x.
  12. 1 2 U.G. Mueller; T.R. Schultz; C.R. Currie; R.M.M. Adams; D. Malloch (2001). "The origin of the attine ant-fungus mutualism". Quarterly Review of Biology. 76 (2): 169–197. PMID 11409051. doi:10.1086/393867.
  13. ↑ Cameron R. Currie; Bess Wong; Alison E. Stuart; Ted R. Schultz; Stephen A. Rehner; Ulrich G. Mueller; Gi-Ho Sung; Joseph W. Spatafora; Neil A. Straus (2003). "Ancient tripartite coevolution in the attine ant-microbe symbiosis". Science. 299 (5605): 386–8. Bibcode:2003Sci...299..386C. PMID 12532015. doi:10.1126/science.1078155.
  14. ↑ Currie, Cameron; et al. (2006). "Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants". Science. 311 (5757): 81–3. Bibcode:2006Sci...311...81C. PMID 16400148. doi:10.1126/science.1119744.
  15. ↑ Little, Ainslie; Cameron Currie (2008). "Black yeast symbionts compromise the efficiency of antibiotic defenses in fungus-growing ants". Ecology. 89 (5): 1216–1222. PMID 18543616. doi:10.1890/07-0815.1.
  16. 1 2 Mikheyev, A. "Convergent coevolution in the domestication of coral mushrooms by fungus-growing ants.". Proceedings of the Royal Society B: Biological Sciences. 271 (1550): 1777–1782. PMC 1691797 Freely accessible. PMID 15315892. doi:10.1098/rspb.2004.2759.
  17. ↑ Little, Ainslie; Cameron Currie (2009). "Parasites may help stabilize cooperative relationships". BMC Evolutionary Biology. 9: 120–124. PMC 2701933 Freely accessible. PMID 19486536. doi:10.1186/1471-2148-9-124.
  18. ↑ Kellner, K; et al. (2013). "Co-evolutionary patterns and diversification of ant–fungus associations in the asexual fungus-farming ant Mycocepurus smithii in Panama". Evolutionary Biology. 26 (6): 1353–1362. doi:10.1111/jeb.12140.
  19. ↑ "The Ghost Ant: New Species is a Living Fossil of Ancient Fungus-Farming Ants". Nature World News. Dec 23, 2013. Retrieved 24 Dec 2013.
  20. 1 2 Mikheyev, S.; U.G. Mueller; P. Abbott (2006). "Cryptic sex and many-to-one coevolution in the fungus-growing ant symbiosis" (PDF). Proceedings of the National Academy of Sciences. 103 (28): 10702–10706. Bibcode:2006PNAS..10310702M. PMC 1502295 Freely accessible. PMID 16815974. doi:10.1073/pnas.0601441103.
  21. ↑ The prominent role of fungi and fungal enzymes in the Ant–fungus biomass conversion symbiosi, National Center for Biotechnology Information, Apr 23, 2014
  22. ↑ B.T.M. Dentinger; D.J. Lodge; A.B. Munkacsi; D.E. Desjardin; D. J. McLaughlin (2009). "Phylogenetic placement of an unusual coral mushroom challenges the classic hypothesis of strict coevolution in the Apterostigma pilosum group ant-fungus mutualism". Evolution. 63 (8): 2172–2178. PMID 19453731. doi:10.1111/j.1558-5646.2009.00697.x.
  23. ↑ A.S. Mikheyev; U.G. Mueller; J.J. Boomsma (2007). "Population genetic signatures of diffuse co-evolution between leaf-cutting ants and their cultivar fungi". Molecular Ecology. 16 (1): 209–216. PMID 17181732. doi:10.1111/j.1365-294X.2006.03134.x.
  24. ↑ Seal, Jon N.; Mueller, U. G. (2013-08-01). "Instability of novel ant-fungal associations constrains horizontal exchange of fungal symbionts". Evolutionary Ecology. 28 (1): 157–176. ISSN 0269-7653. doi:10.1007/s10682-013-9665-8.
  25. ↑ Mehdiabadi, Natasha J.; Hughes, Benjamin; Mueller, Ulrich G. (2006-03-01). "Cooperation, conflict, and coevolution in the attine ant-fungus symbiosis". Behavioral Ecology. 17 (2): 291–296. ISSN 1045-2249. doi:10.1093/beheco/arj028.
  26. ↑ Mehdiabadi, Natasha J.; Mueller, Ulrich G.; Brady, Seán G.; Himler, Anna G.; Schultz, Ted R. (2012-05-15). "Symbiont fidelity and the origin of species in fungus-growing ants". Nature Communications. 3: 840. ISSN 2041-1723. doi:10.1038/ncomms1844.
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