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Fungal Adaptations to Mutualistic Life with Ants

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Fungal Adaptations to Mutualistic Life with Ants faculty of science university of copenhagen centre for social evolution department of biology Fungal adaptations to mutualistic life with ants This thesis dissertation has been submitted in accordance with the requirements for the degree of PhD, at the PhD School of The Faculty of Science, University of Copenhagen, Denmark to be defended publicly before a panel of examiners. by Pepijn W. Kooij December 2013 Academic advisors Prof. Jacobus J. Boomsma Dr. Morten Schiøtt Cover Front: Atta sexdens workers carrying leaves down a tree. Picture: P. W. Kooij, Location: Santa Cruz, Gamboa, Panama Back: incipient colony of Atta colombica with queen on top. Picture: P. W. Kooij, Location: Gamboa, Panama PREFACE This thesis is the result of a three-year PhD project carried out at the Cen- tre for Social Evolution (CSE), Department of Biology, University of Copenhagen in Denmark under the supervision of Professor Jacobus J. Boomsma and Dr. Morten Schiøtt. During the project I spent five weeks at the Laboratory of Genetics, Wagenin- gen University and Research Center, The Netherlands, hosted by Dr. Duur K. Aanen. I additionally carried out a total of seven weeks of fieldwork at the Smithsonian Tropical Research Institute in Panama. I was funded by the Danish National Research Founda- tion and the Department of Biology. The thesis is comprised of a general introduction on the current understand- ing of life-time mutualistic interactions and how this can be applied to my model system where the fungal symbiont adapted to a life-time commitment with ants. I also present the objectives of the thesis research, and conclude with a summary of the main results in a broader conceptual framework. This is followed by five chapters of origi- nal emperical work, one of which is in press in a peer-reviewed journal, one has been submitted to a peer-reviewed journal and three that are in preparation for submission. Pepijn W. Kooij Copenhagen, December, 2013 CONTENTS Summaries.....................................................................................................................................................7 General introduction...................................................................................................................................13 Mutualism, commitment and co-adaptation.............................................................................................14 The fungus-growing ants as model system................................................................................................15 Open questions and objectives of this thesis.............................................................................................17 The influence of domestication on fungal genetics.......................................................................................17 Incompatibility between fungal crops of different ant genera.......................................................................18 Decomposition enzymes in the fungus-growing ant symbiosis....................................................................19 Special Acromyrmex echinatior fungal symbiont enzymes...........................................................................20 Summary and future perspectives.............................................................................................................21 References....................................................................................................................................................27 Chapter 1:....................................................................................................................................................33 Advanced farming ants rear polyploidy crop fungi Chapter 2:....................................................................................................................................................61 Somatic incompatibility of fungal crops in sympatric Atta and Acromyrmex leaf-cutting ants Chapter 3:....................................................................................................................................................85 Differences in forage-acquisition and fungal enzyme activity contribute to niche segregation in Panamanian leaf-cutting ants Chapter 4:...................................................................................................................................................109 Leucoagaricus gongylophorus uses leaf-cutting ants to vector proteolytic enzymes towards new plant sub- strate Chapter 5:...................................................................................................................................................133 Cellulose degradation patterns in Acromyrmex echinatior colonies Acknowledgements...................................................................................................................................153 6 ENGLISH, DANSK, ESPAÑOL, NEDERLANDS SUMMARIES 7 SUMMARY Fungus-growing ants (Attini) feed off a fungus they cultivate in a mutualistic symbiosis in under- ground chambers by providing it substrate they collect outside the colony. The tribe of Attine ants ranges from small colonies of the paleo- and basal Attine species with a few hundred workers that forage on crude substrates such as insect frass and dry plant material, to large colonies of the leaf-cutting ants with several thousands to several million workers that provide live plant material to their fungus gardens. Leaf-cutting ants are the dominant herbivores of the Neo-tropics, and have a major contribution to cycling of nitrogen and phosphorus in their direct environment and are, furthermore, considered pest species as they have a large impact on human agriculture. These factors make leaf-cutting ants an ideal study subject to better understand the mechanisms that make this mutualistic symbiosis so successful. To understand the evolutionary development of domestication of the fungus over the phylogeny of the Attine ants, I compared the average number of nuclei per cell for the fungal symbionts, for each of the different groups of fungus-growing ants. I found that the fungal symbionts of the paleo- and basal Attine ants, which have a relative low level of domestication, have two nuclei per cell, the standard for Basidiomy- cete fungi, but that the average number increased to 7-17 nuclei per cell in the highly domesticated fungi of the higher Attine ants and leaf-cutting ants. Furthermore, I was able to estimate that approximately half of these nuclei were represented by different genomes, giving the fungus a ploidy level of 5n-6n. In mutualistic symbioses it is important the partners stay true to each other. In fungus-growing ants, new founding queens bring a piece of fungus to build up their new colony. However, in rare occa- sions fungal symbionts might come into contact with symbionts from other colonies. I showed that in both leaf-cutting ant genera incompatibility reactions between fungal strains can avoid intermixing of different strains, and that these reactions strengthen when genetic distance is increased. This pattern, however, be- comes distorted when fungal symbionts are contested across ant genera. The most important mechanism in the succession of this mutualism of leaf-cutting ants is the con- trolled degradation of plant material. I show that in the area of Gamboa, Panama, the two leaf-cutting ant genera forage for rather different plant material, with Atta species specializing on tree-leaves and Acromyr- mex focusing more on flower material and herbal plant material. This difference is reflected in the overall enzyme activity patterns in the fungus gardens, with Atta specializing more on specific enzyme groups and Acromyrmex having an overall high enzyme activity. Finally, I show that the fungal symbiont of the leaf-cutting ant Acromyrmex echinatior produces large amounts of biodegrading enzymes in special structures called gongylidia. The ants eat these structures, but enzymes pass the ant gut without being digested, and are excreted by the ants in their fecal fluid which they mix with freshly foraged plant material placed on the top of the fungus garden. The enzymes are still active and have therefore an important role in the biodegradation of the plant material. With this I show that the fungus evolved some incredible adaptations to a mutualistic life with the ants. 8 RESUMÉ Svampedyrkende myrer lever af en svamp de dyrker i en mutualistisk symbiose i underjordiske kamre ved at forsyne den med substrat som de henter udefra. Underfamilien af svampedyrkende myrer (At- tini) spænder over paleo- og basale arter med få hundrede arbejdere der fouragerer på tørret plantemateriale og insekt ekskrementer, til store kolonier af bladskærermyrer med flere tusinde til millioner af arbejdere der indsamler friskt plantemateriale til deres svampehaver. Bladskærermyrer er den dominante herbivor i neotroperne hvor de bidrager væsentligt til nitrogen og fosfor kredsløbet i deres nærmiljø og bliver yder- mere betragtet som et skadedyr idet de har stor effekt på landbruget. Disse faktorer gør det ideelt at benytte bladskærermyrer til bedre at forstå mekanismerne der har gjort denne mutualistiske symbiose så succesfuld. For at forstå udviklingen af domesticeringen af svampen over hele den Attine fylogeni, sam- menlignede jeg det gennemsnitlige antal kerner per celle i svampesymbionten hos forskellige grupper af svampedyrkende myrer. Jeg fandt at svampesymbionten hos myrerne fra paleo- og basale arter, som har relativ lavt niveau
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