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{{short description|Symbiotic relationship}}
{{short description|Symbiotic relationship}}
[[File:Atta colombica queen.jpg|thumb|''[[Atta colombica]]'' queen]]
[[File:Atta colombica queen.jpg|thumb|''[[Atta colombica]]'' queen]]
'''Ant–fungus mutualism''' is a [[symbiosis]] seen between certain [[ant]] and [[fungus|fungal]] species, in which ants actively cultivate fungus much like humans farm [[agriculture|crop]]s as a food source. There is only evidence of two instances in which this form of agriculture evolved in ants resulting in a dependence on fungi for food. These instances were the attine ants and some ants that are part of the megalomyrmex genus. In some species, the ants and fungi are dependent on each other for survival. This type of codependency is prevalent among herbivores who rely on plant material for nutrition. The microbes’ ability to convert the plant material into a food source accessible to their host makes them the ideal partner. The [[leafcutter ant]] is a well-known example of this symbiosis.<ref>{{cite book
'''The ant–fungus mutualism''' is a [[symbiosis]] seen between certain [[ant]] and [[fungus|fungal]] species, in which ants actively cultivate fungus much like humans farm [[agriculture|crop]]s as a food source. There is only evidence of two instances in which this form of agriculture evolved in ants resulting in a dependence on fungi for food. These instances were the attine ants and some ants that are part of the megalomyrmex genus.<ref>{{Cite journal |last=Mueller |first=Ulrich G. |last2=Schultz |first2=Ted R. |last3=Currie |first3=Cameron R. |last4=Adams |first4=Rachelle M. M. |last5=Malloch |first5=David |date=2001 |title=The Origin of the Attine Ant-Fungus Mutualism |url=https://www.jstor.org/stable/2664003 |journal=The Quarterly Review of Biology |volume=76 |issue=2 |pages=169–197 |issn=0033-5770}}</ref> In some species, the ants and fungi are dependent on each other for survival. This type of codependency is prevalent among herbivores who rely on plant material for nutrition. The microbes’ ability to convert the plant material into a food source accessible to their host makes them the ideal partner.<ref>{{Cite journal |last=Aylward |first=Frank O. |last2=Currie |first2=Cameron R. |last3=Suen |first3=Garret |date=2012-03 |title=The Evolutionary Innovation of Nutritional Symbioses in Leaf-Cutter Ants |url=https://www.mdpi.com/2075-4450/3/1/41 |journal=Insects |language=en |volume=3 |issue=1 |pages=41–61 |doi=10.3390/insects3010041 |issn=2075-4450}}</ref> The [[leafcutter ant]] is a well-known example of this symbiosis.<ref>{{cite book
|author1=B. Hölldobler
|author1=B. Hölldobler
|author2=E.O. Wilson
|author2=E.O. Wilson
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|url-access=registration
|url-access=registration
|url=https://archive.org/details/journeytoantss00holl
|url=https://archive.org/details/journeytoantss00holl
}}</ref> Leafcutter ants species span more than one continent, finding homes in southern South America all the way up to the United States. However, ants are not the only ground-dwelling arthropods which have developed symbioses with fungi. A [[Mutualism (biology)|mutualism]] with fungi is also noted in some species of [[termite]]s in [[Africa]].<ref name=Mueller2005>{{Cite journal
}}</ref> Leafcutter ants species span more than one continent, finding homes in southern South America all the way up to the United States.<ref>{{Cite journal |last=Aylward |first=Frank O. |last2=Currie |first2=Cameron R. |last3=Suen |first3=Garret |date=2012-03 |title=The Evolutionary Innovation of Nutritional Symbioses in Leaf-Cutter Ants |url=https://www.mdpi.com/2075-4450/3/1/41 |journal=Insects |language=en |volume=3 |issue=1 |pages=41–61 |doi=10.3390/insects3010041 |issn=2075-4450}}</ref> However, ants are not the only ground-dwelling arthropods which have developed symbioses with fungi. A [[Mutualism (biology)|mutualism]] with fungi is also noted in some species of [[termite]]s in [[Africa]].<ref name=Mueller2005>{{Cite journal
| last1 = Mueller | first1 = U. G.
| last1 = Mueller | first1 = U. G.
| last2 = Gerardo | first2 = N. M.
| last2 = Gerardo | first2 = N. M.
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==Overview==
==Overview==
[[File:Atta Texana incipient garden (41389275364).jpg|thumb|Until the first generation of the new colony is born and matures, the queen will have to cultivate the fungus herself. When a queen is establishing a new colony, she brings a fungal cultivar from her previous colony and lays her eggs around it. Once the eggs mature, she retires from cultivating and continues to lay as many as 20,000 eggs to establish the rest of the colony.<ref>{{Cite journal |last=Weber |first=Neal |date=August 1972 |title=The Fungus-culturing Behavior of Ants |journal=American Zoologist |volume=Volume 12 |pages=577-587}}</ref>]]
⚫
Fungus-growing ants actively propagate, nurture, and defend Lepiotaceae and other lineages of [[basidiomycete]] fungus.<ref name=chapela>{{cite journal
[[File:Atta laevigata fungus garden.jpg|thumb|Atta, "higher attine" ants and their cultivar fungus]]
⚫
Fungus-growing ants actively propagate, nurture, and defend Lepiotaceae and other lineages of [[basidiomycete]] fungus.<ref name="chapela">{{cite journal
|author1=I.H. Chapela |author2=S.A. Rehner |author3=T.R. Schultz |author4=U.G. Mueller |date=9 Dec 1994
|author1=I.H. Chapela |author2=S.A. Rehner |author3=T.R. Schultz |author4=U.G. Mueller |date=9 Dec 1994
|title=Evolutionary history of the symbiosis between fungus-growing ants and their fungi
|title=Evolutionary history of the symbiosis between fungus-growing ants and their fungi
Line 36: Line 38:
|doi=10.1126/science.266.5191.1691
|doi=10.1126/science.266.5191.1691
|pmid=17775630
|pmid=17775630
|bibcode = 1994Sci...266.1691C |s2cid=22831839 }}</ref> In return, the fungus provides nutrients for the ants, which may accumulate in specialized [[hypha]]l-tips known as "gongylidia". In some advanced [[genus|genera]] the [[queen ant]] may take a pellet of the fungus with her when she leaves to start a new colony.<ref>{{cite journal
|bibcode = 1994Sci...266.1691C |s2cid=22831839 }}</ref> In return, the fungus provides nutrients for the ants, which may accumulate in specialized [[hypha]]l-tips known as "gongylidia". These growths are synthesized from plant substrates and are rich in lipids and carbohydrates. In some advanced [[genus|genera]] the [[queen ant]] may take a pellet of the fungus with her when she leaves to start a new colony.<ref>{{cite journal
|author=N. Weber
|author=N. Weber
|year=1966
|year=1966
Line 47: Line 49:
|pmid=17757227
|pmid=17757227
|bibcode = 1966Sci...153..587W |s2cid=31919824
|bibcode = 1966Sci...153..587W |s2cid=31919824
}}</ref> There are three castes of female worker ants in Attini colonies which all participate in foraging plant matter to feed the fungal cultivar. The lowest caste, minor, is smallest in size but largest in number and is primarily responsible for maintaining the fungal cultivar<ref name=":0">{{Citation |last=Boulogne |first=Isabelle |title=Leaf-Cutting Ants, Biology and Control |date=2014 |url=https://doi.org/10.1007/978-3-319-00915-5_1 |work=Sustainable Agriculture Reviews: Volume 13 |pages=1–17 |editor-last=Lichtfouse |editor-first=Eric |place=Cham |publisher=Springer International Publishing |language=en |doi=10.1007/978-3-319-00915-5_1&sa=d&source=docs&ust=1650898126407858&usg=aovvaw3fgih6iixv9ooj_el12lkj |isbn=978-3-319-00915-5 |access-date=2022-04-25 |last2=Ozier-Lafontaine |first2=Harry |last3=Loranger-Merciris |first3=Gladys}}</ref> for the rest of the colony. The symbiosis between basidiomycete fungi and attine ants involves the fungal pathogen, Escovopsis, and an actinomycetes bacterial symbiont, pseudonocardia.<ref name=":0" /> This indicates that the evolutionary relationship is not restricted between fungus and ants but incorporates a community of symbionts.<ref name=":0" />
}}</ref>


==Types==
==Types==

Revision as of 14:02, 25 April 2022

Atta colombica queen

The ant–fungus mutualism is a symbiosis seen between certain ant and fungal species, in which ants actively cultivate fungus much like humans farm crops as a food source. There is only evidence of two instances in which this form of agriculture evolved in ants resulting in a dependence on fungi for food. These instances were the attine ants and some ants that are part of the megalomyrmex genus.[1] In some species, the ants and fungi are dependent on each other for survival. This type of codependency is prevalent among herbivores who rely on plant material for nutrition. The microbes’ ability to convert the plant material into a food source accessible to their host makes them the ideal partner.[2] The leafcutter ant is a well-known example of this symbiosis.[3] Leafcutter ants species span more than one continent, finding homes in southern South America all the way up to the United States.[4] However, ants are not the only ground-dwelling arthropods which have developed symbioses with fungi. A mutualism with fungi is also noted in some species of termites in Africa.[5]

Overview

Until the first generation of the new colony is born and matures, the queen will have to cultivate the fungus herself. When a queen is establishing a new colony, she brings a fungal cultivar from her previous colony and lays her eggs around it. Once the eggs mature, she retires from cultivating and continues to lay as many as 20,000 eggs to establish the rest of the colony.[6]
Atta, "higher attine" ants and their cultivar fungus

Fungus-growing ants actively propagate, nurture, and defend Lepiotaceae and other lineages of basidiomycete fungus.[7] In return, the fungus provides nutrients for the ants, which may accumulate in specialized hyphal-tips known as "gongylidia". These growths are synthesized from plant substrates and are rich in lipids and carbohydrates. In some advanced genera the queen ant may take a pellet of the fungus with her when she leaves to start a new colony.[8] There are three castes of female worker ants in Attini colonies which all participate in foraging plant matter to feed the fungal cultivar. The lowest caste, minor, is smallest in size but largest in number and is primarily responsible for maintaining the fungal cultivar[9] for the rest of the colony. The symbiosis between basidiomycete fungi and attine ants involves the fungal pathogen, Escovopsis, and an actinomycetes bacterial symbiont, pseudonocardia.[9] This indicates that the evolutionary relationship is not restricted between fungus and ants but incorporates a community of symbionts.[9]

Types

There are five main types of agriculture that fungus-growing ants practice:[10] 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.[11][12] Coral-fungus agriculture is practiced by 34 species by a single derived clade within the genus Apterostigma.[12] The coral fungus farmers underwent a switch of cultivars between 10 and 20 million years ago to a non-leucocoprineaceous fungus, which makes its choice of cultivar different from all other attines.[13][14] 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.[14] Generalized higher agriculture is practiced by 63 species in two genera and refers to the condition of highly domesticated fungus.[12] 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.[14] 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.[14] Leaf cutters use living biomass as the substrate to feed their fungi, whereas in all other types of agriculture, the fungus requires dead biomass.[14]

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.[5][7][15] 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.[16] 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.[5][17]

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.[18] In fact, some species of ants have evolved exocrine glands that apparently nourish the antibiotic-producing bacteria inside them.[19] 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.[20]

Partner fidelity

Partner fidelity can be witnessed through vertical gene transmission of fungi when a new colony is begun.[21] 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 they 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.[22] 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.[23] 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.[21]

Evolution

Given the exclusive New World distribution of the over 200 fungus-growing ant species,[17] 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-gatherer grew scarce. At the same time, the sister group of the attine ants Dacetina developed predatory behavior during the same drive for new resources.[24] The 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.[25] The species Cyatta abscondita is considered the most recent ancestor of all leaf-cutting ants.[26]

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.[7] 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.[27]

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.[28] 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.[29] 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.[30]

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.[31] 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.[32][33] 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[34] and strong host-symbiont specificity[11][27] 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.[35] The alternative perspective of a "tight" coevolution points to evidence of instability in horizontal transmission events,[36][37] while also postulating that the observed differences between the phylogenies of attine ants and their fungal cultivars correspond to speciation events.[38]

See also

References

  1. ^ Mueller, Ulrich G.; Schultz, Ted R.; Currie, Cameron R.; Adams, Rachelle M. M.; Malloch, David (2001). "The Origin of the Attine Ant-Fungus Mutualism". The Quarterly Review of Biology. 76 (2): 169–197. ISSN 0033-5770.
  2. ^ Aylward, Frank O.; Currie, Cameron R.; Suen, Garret (2012-03). "The Evolutionary Innovation of Nutritional Symbioses in Leaf-Cutter Ants". Insects. 3 (1): 41–61. doi:10.3390/insects3010041. ISSN 2075-4450. {{cite journal}}: Check date values in: |date= (help)CS1 maint: unflagged free DOI (link)
  3. ^ B. Hölldobler; E.O. Wilson (1990). The Ants. Cambridge MA: Belknap. ISBN 978-0-674-48525-9.
  4. ^ Aylward, Frank O.; Currie, Cameron R.; Suen, Garret (2012-03). "The Evolutionary Innovation of Nutritional Symbioses in Leaf-Cutter Ants". Insects. 3 (1): 41–61. doi:10.3390/insects3010041. ISSN 2075-4450. {{cite journal}}: Check date values in: |date= (help)CS1 maint: unflagged free DOI (link)
  5. ^ a b c 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. S2CID 32500168.
  6. ^ Weber, Neal (August 1972). "The Fungus-culturing Behavior of Ants". American Zoologist. Volume 12: 577–587. {{cite journal}}: |volume= has extra text (help)
  7. ^ a b c 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. doi:10.1126/science.266.5191.1691. PMID 17775630. S2CID 22831839.
  8. ^ N. Weber (1966). "Fungus-growing Ants". Science. 153 (3736): 587–604. Bibcode:1966Sci...153..587W. doi:10.1126/science.153.3736.587. PMID 17757227. S2CID 31919824.
  9. ^ a b c Boulogne, Isabelle; Ozier-Lafontaine, Harry; Loranger-Merciris, Gladys (2014), Lichtfouse, Eric (ed.), "Leaf-Cutting Ants, Biology and Control", Sustainable Agriculture Reviews: Volume 13, Cham: Springer International Publishing, pp. 1–17, doi:10.1007/978-3-319-00915-5_1&sa=d&source=docs&ust=1650898126407858&usg=aovvaw3fgih6iixv9ooj_el12lkj, ISBN 978-3-319-00915-5, retrieved 2022-04-25
  10. ^ 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.
  11. ^ a b 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. doi:10.1073/pnas.0711024105. PMC 2291119. PMID 18362345.
  12. ^ a b c Mehdiabdi and Schultz 2009
  13. ^ "Evolution of ant-cultivar specialization and cultivar switching in Apterostigma fungus-growing ants". Evolution. 58 (10): 2252–2265. 2004. doi:10.1554/03-203. PMID 15562688. S2CID 19442271. {{cite journal}}: Unknown parameter |authors= ignored (help)
  14. ^ a b c d e Schultz and Brady 2008
  15. ^ Weber N. A. 1972. Gardening ants: The attines. Philadelphia (PA): American Philosophical Society.
  16. ^ 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 (4): 337–370. doi:10.1111/j.1365-3113.1995.tb00100.x. S2CID 86455302.
  17. ^ a b 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. doi:10.1086/393867. PMID 11409051. S2CID 19465007.
  18. ^ 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. doi:10.1126/science.1078155. PMID 12532015. S2CID 15815635.
  19. ^ 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. CiteSeerX 10.1.1.186.9613. doi:10.1126/science.1119744. PMID 16400148. S2CID 8135139.
  20. ^ Little, Ainslie; Cameron Currie (2008). "Black yeast symbionts compromise the efficiency of antibiotic defenses in fungus-growing ants". Ecology. 89 (5): 1216–1222. doi:10.1890/07-0815.1. PMID 18543616. S2CID 28969854.
  21. ^ a b Mikheyev, A (2004). "Convergent coevolution in the domestication of coral mushrooms by fungus-growing ants". Proceedings of the Royal Society B: Biological Sciences. 271 (1550): 1777–1782. doi:10.1098/rspb.2004.2759. PMC 1691797. PMID 15315892.
  22. ^ Little, Ainslie; Cameron Currie (2009). "Parasites may help stabilize cooperative relationships". BMC Evolutionary Biology. 9: 120–124. doi:10.1186/1471-2148-9-124. PMC 2701933. PMID 19486536.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  23. ^ Kellner, K; et al. (2013). "Co-evolutionary patterns and diversification of ant–fungus associations in the asexual fungus-farming ant Mycocepurus smithii in Panama". Journal of Evolutionary Biology. 26 (6): 1353–1362. doi:10.1111/jeb.12140. PMID 23639137. S2CID 23711609.
  24. ^ Branstetter, M. G.; Ješovnik, J.; Sosa-Calvo, M. W.; Lloyd, B.C.; Brady, S.G.; Shultz, T.R. (2017). "Dry habitats were crucibles of domestication in the evolution of agriculture in ants". Proceedings of the Royal Society B: Biological Sciences. 284 (1852): 20170095. doi:10.1098/rspb.2017.0095. PMC 5394666. PMID 28404776.
  25. ^ Nygaard, S; Li, M; Schiøtt, Z; Chen, z; Yang, Q; Xie; et al. (2016). "Reciprocal genomic evolution in the ant-fungus agriculutural synthesis". Nature Communications. 7: 12233. doi:10.1038/ncomms12233. PMC 4961791. PMID 27436133.
  26. ^ "The Ghost Ant: New Species is a Living Fossil of Ancient Fungus-Farming Ants". Nature World News. Dec 23, 2013. Retrieved 24 Dec 2013.
  27. ^ a b 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. doi:10.1073/pnas.0601441103. PMC 1502295. PMID 16815974.
  28. ^ The prominent role of fungi and fungal enzymes in the Ant–fungus biomass conversion symbiosi, National Center for Biotechnology Information, Apr 23, 2014
  29. ^ Nygaard, S. H.; Hu, C; Li, M; Schiøtt, Z; Chen, Z; Yang, Q; Zie (2016). "Reciprocal genomic evolution in the ant–fungus agricultural symbiosis". Nature Communications. 7: 122233. Bibcode:2016NatCo...712233N. doi:10.1038/ncomms12233. PMC 4961791. PMID 27436133.
  30. ^ Nygaard, S. H.; Hu, C; Li, M; Schiøtt, Z; Chen, Z; Yang, Q; Zie (2016). "Reciprocal genomic evolution in the ant–fungus agricultural symbiosis". Nature Communications. 7: 122233. Bibcode:2016NatCo...712233N. doi:10.1038/ncomms12233. PMC 4961791. PMID 27436133.
  31. ^ Nygaard, S. H.; Hu, C; Li, M; Schiøtt, Z; Chen, Z; Yang, Q; Zie (2016). "Reciprocal genomic evolution in the ant–fungus agricultural symbiosis". Nature Communications. 7: 122233. Bibcode:2016NatCo...712233N. doi:10.1038/ncomms12233. PMC 4961791. PMID 27436133.
  32. ^ Branstetter, M. G.; Ješovnik, J.; Sosa-Calvo, M. W.; Lloyd, B.C.; Brady, S.G.; Shultz, T.R. (2017). "Dry habitats were crucibles of domestication in the evolution of agriculture in ants". Proceedings of the Royal Society B: Biological Sciences. 284 (1852): 20170095. doi:10.1098/rspb.2017.0095. PMC 5394666. PMID 28404776.
  33. ^ Nygaard, S. H.; Hu, C; Li, M; Schiøtt, Z; Chen, Z; Yang, Q; Zie (2016). "Reciprocal genomic evolution in the ant–fungus agricultural symbiosis". Nature Communications. 7: 122233. Bibcode:2016NatCo...712233N. doi:10.1038/ncomms12233. PMC 4961791. PMID 27436133.
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  35. ^ 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. doi:10.1111/j.1365-294X.2006.03134.x. PMID 17181732. S2CID 12600583.
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