The Occasional Hymenoptera: Leaf-cutter genome and new brain-manipulating fungi

Two new papers have been published in the open access Public Library of Science online journal which relate to ant topics we have recently commented on.

1. Garret Suen, Clotilde Teiling, Lewyn Li, Carson Holt, Ehab Abouheif, et al., “The Genome Sequence of the Leaf-Cutter Ant Atta cephalotes Reveals Insights into Its Obligate Symbiotic Lifestyle,” PLoS Genetics 7(2): e1002007 (February 10, 2011), reports on the results of DNA sequencing of three males from a mature Atta cephalotes colony in Gamboa, Panama. Attine ants are of course the leaf-cutter ants which cultivate fungal gardens for their basic nutrition supply. We’ve seen these ants also in connection with the antibiotics they cultivate to inoculate the fungus as well as how the foragers are “retired” once their mandibles are worn.

The method employed was pyrosequencing (using the FLX Titanium platform of 454 Life Sciences), and the authors performed 12 whole-genome shotgun fragment runs as well as two 8 kpb and one 20 kpb paired-end sequencing runs. The result of assembling this data was a genome of 290 million base pairs (Mbp) which was close to the estimated genome of 300 Mbp. A variety of tests suggested that the genome recovered was complete.

(a) Leaf cutter ants harvest leaves, which become (b) substrate for fungal gardens. (c) The diverse morphology represent a caste system based on functions, from foragers to gardeners to soldiers, etc. From Suet paper. Photo Credits: (a) Jarrod J. Scott/University of Wisconsin-Madison; (b) Austin D. Lynch/University of Wisconsin-Madison. Click to enlarge.

The authors compared the presence, absence and duplication of a number of genes of A. cephalotes with those of other insects and came to a variety of hypotheses of the role of different genes in wing development (or not) in different castes, insulin signaling and caste differentiation, production of cuticular hydrocarbons, which are thought to enable recognition of colony mates, and other genetic bases for aspects of eusocial behavior.

The aspect of the leaf-cutter genome that the authors make special reference to is the absence of two genes necessary for certain biosynthesis. The authors constructed a map of the pathway for biosynthesis of argentine based on the genomes of four other hymenopterans: the ants Camponotus floridanus (the Florida carpenter ant) and Harpegnathos saltator (a “primitive” ant), the honey bee Apis mellifera, and the solitary parasitic jewel wasp Nasonia vitripennis. Based on the map, the leaf-cutter Atta cephalotes lacks two enzymes (agininosuccinate synthase and argininosuccinate lyase) which are necessary for the conversion of aspartate and citrulline into the common amino acid arginine. In addition the leaf cutter seems to have lost the need to rely on certain hexamerins (storage proteins found in the other four hymenopterans) as a source of amino acids during larval development.

The explanation suggested is that the enzymes or the amino acids are provided by the fungal cultivar raised by the leaf-cutters. This of course would reflect the obligate symbiotic life-style of the leaf-cutter. But it also raises the question of how as a matter of natural selection a genetic ability is “lost.” Not having the ability to synthesize argentine may not be “necessary” given the ants’ cultivation of fungus, but that doesn’t explain why not having the ability gave differential reproductive success over ants that retained the ability. On first glance it would seem that an ability to synthesize a necessary amino acid, even if redundant, would nevertheless confer at least a slight survival advantage, for instance when a pathogen severely reduced the fungal garden. The authors suggest that the genetic reductions helped “stabilize” the mutualistic relationship. And perhaps it is true that it will take a more complete understanding of both host-microbe symbiosis and eusociality in hymenopterans before any explanation of loss of these abilities can be attempted.

2. Harry C. Evans, Simon L. Elliot & David P. Hughes, “Hidden Diversity Behind the Zombie-Ant Fungus Ophiocordyceps unilateralis: Four New Species Described from Carpenter Ants in Minas Gerais, Brazil,” PLoS ONE 6(3): e17024 (March 2, 2011), reports on the discovery of four new species of the fungus that is responsible for causing “zombie” behavior in tropical carpenter ants. The newly described fungi were collected in the Atlantic rainforest in the south-eastern region (Zona da Mata) of the State of Minas Gerais, Brazil.

We previously discussed the complicated systematics relating to the Ophiocordyceps complex based on the work of Gi-Ho Sung. The new species are specific to particular carpenter ant hosts: Camponotus rufipesC. balzaniC. melanoticus and C. novogranadensis. The authors show how the new species can be separated using traditional micromorphology. They name the new species after their respective hosts.

a) Original plate from the 1865 Selecta Fungorum Carpologia of the Tulasne brothers, illustrating the holotype of Torrubia unilateralis; b) Detail from plate showing the distinctive pronotal plate of Camponotus sericeiventris; c) Live worker of C. sericeiventris showing the spines on the pronotal plate (arrow). Figure 1 of Evans paper. Click to enlarge.

For fans of complex taxonomic histories, the paper sets out how the fungus group was originally described. The first zombie-inducing fungus was originally called Torrubia unilateralis in an 1865 article published in France by the Tulasne brothers. I have not been able to track down the article, nor would I have the patience to translate the “scientific” Latin it is written in, so I rely on the description of it in the Evans paper. The paper said that the holotype, which was then held at the Museum of Entomology in Paris, was taken from the leaf-cutting ant Atta cephalotes from Brazil. The illustration which accompanies the original Tulasne paper, however, clearly shows that the host was a carpenter ant, not a leaf-cutter. Based on the distinctive pronotal plate (shown by the red arrow in the illustration on the left), Ernst Mayr identified the ant species as Camponotus sericeiventris. The original specimen has been lost in the Paris museum for 150 years, but during that time this type of entomopathogenic fungus has been associated only with carpenter ants (ants of the tribe Camponotini) and never with leaf-cutter ants. I’ll refer you to my earlier thumb-nail sketch of the work of Gi-Ho Sung for the more recent work on the taxonomy of these kinds of fungus. Or you can read his work in Studies in Mycology, in the paper entitled “Phylogenetic classification of Cordyceps and the clavicipitaceous fungi,” which is open access (full article).

As for the four newly described species, I’ll refer you directly to the Evans paper. The authors give detailed descriptions of the fungus and more importantly provide gruesome pictures of the short-work they make of their ant hosts. The authors make the suggestion that “ant ecology drives the functional morphology of the fungal pathogen,” but they don’t begin to explain in what respects that principle operates. Nevertheless, they hope that understanding “the diversity of O. unilateralis s.l. at the global level … will allow us to look beyond the ant-infecting Ophiocordyceps and ask how specialised are other species of Ophiocordyceps attacking members of diverse insect orders from the Orthoptera to Lepidoptera.” That perhaps is an ambitious suggestion in the circumstances, but that observation is no criticism of the detailed descriptive work they did on these new fungus species.

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