ATTINE ANTS have been a theme at my blog recently. They first showed up in a discussion of their evolutionary tree, then in a post examining their relationship with the actinomycete bacteria that help protect their fungal gardens from parasites. In my reading I stumbled across the article that I will write about today, which seems to have discovered another part to the attine ant symbiosis. As of now this is the sole report on the occurrence of black yeasts living apparently parasitically on the attine ants, reliant upon the cuticular crypts that normally house helpful actinomycetes.
To recap, the attine ants cultivate fungal gardens and eat these fungi. A different fungus called Escovopsis finds these gardens delicious, and can destroy a garden if it is unprotected. The ants protect their gardens by constant cleaning of the fungi and by growing actinomycete bacteria upon their cuticles that produce antifungal agents. The ants evolved crypts in their cuticles to house these bactera and exocrine glands to support their growth. According to Currie and Little, it appears that some species of black yeast have found these crypts inviting and moved in as well.
Currie and Little cultured black yeasts from Apterostigma ants (incidentally, paleoattine coral fungus farmers) of various species. Attempts to culture the yeasts from other ant genera were unsuccessful, but PCR amplification showed the presence of black yeast DNA on multiple other species of attine ants as well. The yeasts were monophyletic, suggesting that their ancestor made the jump to growing upon ants’ chests once, and that these yeasts descended from those fungi. They were collected from multiple locations in South America, showing that the yeast has a wide geographical distribution. Since these fungi are monophyletic, widespread, and occur in both paleoattine and neoattine ants, the authors suggest they were present early in attine ant evolution.
On Apterostigma workers the yeasts were localized in those areas bearing crypts that house mutualistic actinomycetes. The authors report that the yeasts inhibit actinomycete effectiveness in suppressing Escovopsis, but unfortunately that paper has not been published yet (at least not that I can find). This would make the black yeasts parasites upon the attine ant/actinomycete symbiosis. Apparently the black yeasts find attine cuticular crypts inviting homes. It is unclear whether these yeasts have any detrimental effects upon the ants besides harming the health of their fungal gardens.
The authors suggest four possible routes for the acquisition of black yeasts:
- Since a closely related yeast genus, Phialophora, lives endophytically in plants, the yeast may have been transported into ant colonies in leaves used as fertilizer for fungus gardens.
- The association between ants and black yeasts may have pre-dated the evolution of fungus farming, similarly to how non-farming ants may carry actinomycete bacteria on their integuments.
- The black yeasts may have jumped hosts, perhaps from bark beetles to ants.
- The black yeasts may have an association with Pseudonocardia bacteria that pre-dates the mutualistic relationship of these bacteria with ants. Maybe the yeasts are a “third wheel” that the ants have not yet successfully ejected.
The black yeasts represent a new avenue for research in attine ant ecology. I look forward to seeing more about these possibilities in future articles.
Little, A.E., Currie, C.R. (2007). Symbiotic complexity: discovery of a fifth symbiont in the attine ant-microbe symbiosis. Biology Letters, 3(5), 501-504. DOI: 10.1098/rsbl.2007.0253
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April 7, 2008 at 1:16 pm
Ford
OK, maybe this answers my earlier question. The black yeasts compete with the actinomycetes for crypt resources. That imposes selection on the bacteria (at the level of the individual bacterium or clone, as opposed to the level of the ant colony, where benefits would be shared with nonproducing cheaters) to produce antifungal compounds. Compounds that kill yeast also happen to kill Escovopsis. But I still don’t understand why they don’t kill the food fungi as well.
April 7, 2008 at 2:54 pm
Nimravid
We really don’t know very much right now about this symbiotic network. While we don’t know what compounds these bacteria are producing, we do know that they are specific for Escovopsis, do not harm the cultivars (actually stimulate growth), and haven’t had much success suppressing other fungi studied. Since the presence of black yeast seems to decrease the effectiveness of the bacteria (per the currently unpublished paper mentioned in the paper above), my thoughts would be that either the black yeasts out-compete the bacteria and lower their number or that black yeasts force selection for production of anti-fungals targeted at the yeast instead of Escovopsis.
Certainly the bacteria not killing the cultivar makes sense, because the selection in this case would be upon the ants. If you play host to bacteria that destroy your fungal garden, your genes (passed on by the queen, who is now starving to death) won’t be very successful.
I’m interested in seeing what compound(s) the actinomycetes make, but am afraid there may not be sufficient interest to see that isolated and characterized any time soon.
April 7, 2008 at 5:04 pm
Ford
Interesting. But if the compounds are that specific, then we need some other solution to the tragedy of the commons.
The problem is that bacterial generations are so short relative to the life of an ant colony. So, sure, ant colonies with the wrong bacteria will die out, but that future prospect will have no effect on the evolution of bacteria on the surface of an individual ant. Natural selection has no foresight. Why don’t mutants that divert resources to their own reproduction, at the expense of making antifungals, displace more “altruistic” bacteria?
I can understand why natural selection might favor production of a broad-spectrum antibiotic that would kill within-crypt competitors, with killing Escovopsis as a side effect. (Similarly, root surface bacteria make antibiotics to protect themselves from protozoa, with protection of the plant from fungi as a side-effect.) But how does a strain making something that only kills Escovopsis benefit, relative to competing bacteria in the same crypt that either put their energy into reproducing or make something that kills competing bacteria instead?
Could individual ants somehow tell when they’re carrying less-beneficial strains? If so, they could gain an inclusive fitness benefit by leaving the colony, maybe even trying to contaminate a competing colony…
November 26, 2012 at 1:44 am
eliminating yeast
A quick red wolf jumped over the lazy dog