Ecology and Evolution of Cooperative Fungiculture in Beetles

• Applicant: Professor Dr. Peter Biedermann
• Subject Area: Evolution, Anthropology ; Animal Physiology and Biochemistry ; Sensory and Behavioural Biology
• Term: from 2016 to 2023
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 322563882

• Final Report Year: 2023

Final Report Abstract

Cooperation is ubiquitous in nature and its evolution has challenged generations of evolutionary biologists. Today many principles of social evolution are widely accepted, but major issues remain unsolved. For example, the strongest approach in evolutionary biology, namely experimental evolution of a trait, has not been accomplished for social behaviour in animals. Likewise, fungiculture of some social insects may give us ideas for our human agriculture in terms of the promotion of our crops and the specific suppression of pathogens. In this Emmy-Noether project we used various bark- and ambrosia beetle species and various methodological approaches from behavioural studies, experimental evolution, chemical analyses, ecological stoichiometry, microbial and olfactory bioassays to modern sequencing technologies to address these major questions above and some minor questions regarding the social behaviour, the interactions between social behaviour and fungal mutualism and interactions between bacterial and fungal symbionts. Even though we were unable to select for higher sociality in ambrosia beetles using two different approaches, we discovered that ambrosia beetles can identify their different symbionts by their volatiles and are able to actively promote the growth of their cultivars over fungal competitors. They indirectly do this by selecting an ethanol-rich wood substrate on which their cultivars are better able to outcompete competitors. Furthermore, they are associated with (i) Streptomycetes bacteria that selectively inhibit all fungi except for their cultivars and with (ii) Pseudomonas bacteria that trigger fungal cultivars to fruit by producing a lipopolysaccharide. Generally, we found strong indications that symbiont management is the strongest evolutionary driver for social behaviour in ambrosia beetles and their social systems are limited by the longevity of the wood substrate. After discovering the important role of microbial management in ambrosia beetles, we propose that the interactions with microbes may be an underestimated factor for the evolution of sociality also on other social insects.

Publications

• Evolutionary feedbacks between insect sociality and microbial management. Current Opinion in Insect Science, 22, 92-100.
  Biedermann, Peter H. W. & Rohlfs, Marko
  
• Insect-Fungus Interactions in Dead Wood Systems. Zoological Monographs, 377-427.
  Birkemoe, Tone; Jacobsen, Rannveig M.; Sverdrup-Thygeson, Anne & Biedermann, Peter H. W.
  
• Low intraspecific genetic diversity indicates asexuality and vertical transmission in the fungal cultivars of ambrosia beetles. Fungal Ecology, 32, 57-64.
  van de Peppel, L.J.J.; Aanen, D.K. & Biedermann, P.H.W.
  
• Symbiont selection via alcohol benefits fungus farming by ambrosia beetles. Proceedings of the National Academy of Sciences, 115(17), 4447-4452.
  Ranger, Christopher M.; Biedermann, Peter H. W.; Phuntumart, Vipaporn; Beligala, Gayathri U.; Ghosh, Satyaki; Palmquist, Debra E.; Mueller, Robert; Barnett, Jenny; Schultz, Peter B.; Reding, Michael E. & Benz, J. Philipp
  
• Bark Beetle Population Dynamics in the Anthropocene: Challenges and Solutions. Trends in Ecology & Evolution, 34(10), 914-924.
  Biedermann, Peter H.W.; Müller, Jörg; Grégoire, Jean-Claude; Gruppe, Axel; Hagge, Jonas; Hammerbacher, Almuth; Hofstetter, Richard W.; Kandasamy, Dineshkumar; Kolarik, Miroslav; Kostovcik, Martin; Krokene, Paal; Sallé, Aurélien; Six, Diana L.; Turrini, Tabea; Vanderpool, Dan; Wingfield, Michael J. & Bässler, Claus
  
• Evolutionary chemo-ecology of insect-fungus interactions: Still in its infancy but advancing. Fungal Ecology, 38, 1-6.
  Biedermann, Peter H.W.; De Fine Licht, Henrik H. & Rohlfs, Marko
  
• Fungi associated with beetles dispersing from dead wood – Let's take the beetle bus!. Fungal Ecology, 39, 100-108.
  Seibold, Sebastian; Müller, Jörg; Baldrian, Petr; Cadotte, Marc W.; Štursová, Martina; Biedermann, Peter H.W.; Krah, Franz-Sebastian & Bässler, Claus
  
• Molecular identification and enzymatic profiling of Trypodendron (Curculionidae: Xyloterini) ambrosia beetle-associated fungi of the genus Phialophoropsis (Microascales: Ceratocystidaceae). Fungal Ecology, 38, 89-97.
  Lehenberger, Maximilian; Biedermann, Peter H.W. & Benz, J. Philipp
  
• Pathogen defence is a potential driver of social evolution in ambrosia beetles. Proceedings of the Royal Society B: Biological Sciences, 286(1917), 20192332.
  Nuotclà, Jon A.; Biedermann, Peter H. W. & Taborsky, Michael
  
• Cooperative Breeding in the Ambrosia Beetle Xyleborus affinis and Management of Its Fungal Symbionts. Frontiers in Ecology and Evolution, 8.
  Biedermann, Peter H. W.
  
• Cycloheximide-Producing Streptomyces Associated With Xyleborinus saxesenii and Xyleborus affinis Fungus-Farming Ambrosia Beetles. Frontiers in Microbiology, 11.
  Grubbs, Kirk J.; Surup, Frank; Biedermann, Peter H. W.; McDonald, Bradon R.; Klassen, Jonathan L.; Carlson, Caitlin M.; Clardy, Jon & Currie, Cameron R.
  
• Ecology and Evolution of Insect–Fungus Mutualisms. Annual Review of Entomology, 65(1), 431-455.
  Biedermann, Peter H.W. & Vega, Fernando E.
  
• Evidence for Succession and Putative Metabolic Roles of Fungi and Bacteria in the Farming Mutualism of the Ambrosia Beetle Xyleborus affinis. mSystems, 5(5).
  Ibarra-Juarez, L. A.; Burton, M. A. J.; Biedermann, P. H. W.; Cruz, L.; Desgarennes, D.; Ibarra-Laclette, E.; Latorre, A.; Alonso-Sánchez, A.; Villafan, E.; Hanako-Rosas, G.; López, L.; Vázquez-Rosas-Landa, M.; Carrion, G.; Carrillo, D.; Moya, A. & Lamelas, A.
  
• Four mycangium types and four genera of ambrosia fungi suggest a complex history of fungus farming in the ambrosia beetle tribe Xyloterini. Mycologia, 112(6), 1104-1137.
  Mayers, Chase G.; Harrington, Thomas C.; Mcnew, Douglas L.; Roeper, Richard A.; Biedermann, Peter H. W.; Masuya, Hayato & Bateman, Craig C.
  
• On interactions, associations, mycetangia, mutualists and symbiotes in insect-fungus symbioses. Fungal Ecology, 44, 100909.
  Vega, Fernando E. & Biedermann, Peter H.W.
  
• Social Beetles. Encyclopedia of Social Insects, 1-8.
  Biedermann, Peter H. W. & Nuotclà, Jon A.
  
• Ethanol-Enriched Substrate Facilitates Ambrosia Beetle Fungi, but Inhibits Their Pathogens and Fungal Symbionts of Bark Beetles. Frontiers in Microbiology, 11.
  Lehenberger, Maximilian; Benkert, Markus & Biedermann, Peter H. W.
  
• Habitat Quality Determines Dispersal Decisions and Fitness in a Beetle – Fungus Mutualism. Frontiers in Ecology and Evolution, 9.
  Nuotclà, Jon Andreja; Diehl, Janina Marie Christin & Taborsky, Michael
  
• Microbial Drivers of Sociality – from Multicellularity to Animal Societies. Frontiers Research Topics. Frontiers Media SA.
  McMahon, Dino; Biedermann, Peter H. W.; Rohlfs, Marko & Meunier, Joël (Eds.)
  
• Nutrient-Poor Breeding Substrates of Ambrosia Beetles Are Enriched With Biologically Important Elements. Frontiers in Microbiology, 12.
  Lehenberger, Maximilian; Foh, Nina; Göttlein, Axel; Six, Diana & Biedermann, Peter H. W.
  
• Recent advances toward the sustainable management of invasive Xylosandrus ambrosia beetles. Journal of Pest Science, 94(3), 615-637.
  Gugliuzzo, Antonio; Biedermann, Peter H. W.; Carrillo, Daniel; Castrillo, Louela A.; Egonyu, James P.; Gallego, Diego; Haddi, Khalid; Hulcr, Jiri; Jactel, Hervé; Kajimura, Hisashi; Kamata, Naoto; Meurisse, Nicolas; Li, You; Oliver, Jason B.; Ranger, Christopher M.; Rassati, Davide; Stelinski, Lukasz L.; Sutherland, Roanne; Tropea, Garzia Giovanna ... & Biondi, Antonio
  
• Enhancing the structural diversity between forest patches—A concept and real‐world experiment to study biodiversity, multifunctionality and forest resilience across spatial scales. Global Change Biology, 29(6), 1437-1450.
  Müller, Jörg; Mitesser, Oliver; Cadotte, Marc W.; van der Plas, Fons; Mori, Akira S.; Ammer, Christian; Chao, Anne; Scherer‐Lorenzen, Michael; Baldrian, Petr; Bässler, Claus; Biedermann, Peter; Cesarz, Simone; Claßen, Alice; Delory, Benjamin M.; Feldhaar, Heike; Fichtner, Andreas; Hothorn, Torsten; Kuenzer, Claudia; Peters, Marcell K. ... & Eisenhauer, Nico
  
• Evolutionary ecology of the bark beetlesIps typographusandPityogenes chalcographus. Bulletin of Entomological Research, 113(1), 1-10.
  Schebeck, Martin; Schopf, Axel; Ragland, Gregory J.; Stauffer, Christian & Biedermann, Peter H. W.
  
• First experimental evidence for active farming in ambrosia beetles and strong heredity of garden microbiomes. Proceedings of the Royal Society B: Biological Sciences, 289.
  Diehl, Janina M. C.; Kowallik, Vienna; Keller, Alexander & Biedermann, Peter H. W.
  
• Mycangia Define the Diverse Ambrosia Beetle–Fungus Symbioses. The Convergent Evolution of Agriculture in Humans and Insects, 105-142.
  Mayers, Chase G.; Harrington, Thomas C. & Biedermann, Peter H. W.
  
• Comparing the succession of microbial communities throughout development in field and laboratory nests of the ambrosia beetle Xyleborinus saxesenii. Frontiers in Microbiology, 14.
  Diehl, Janina M. C.; Keller, Alexander & Biedermann, Peter H. W.
  
• Diversity of beetles and associated microorganisms. Frontiers Research Topics.
  Fukatsu, Takema; Biedermann, Peter H. W. & Salem, Hassan (Eds.)
  
• Fidelity or love the one you're with? Biotic complexity and tradeoffs can drive strategy and specificity in beetle‐fungus by‐product mutualisms. Ecology and Evolution, 13(7).
  Six, Diana L. & Biedermann, Peter H. W.
  
• Friend or foe: Ambrosia beetle response to volatiles of common threats in their fungus gardens. Symbiosis, 89(3), 353-358.
  Diehl, Janina M. C.; Kassie, Denicia & Biedermann, Peter H. W.
  
• Highly Diverse Cuticular Hydrocarbon Profiles but No Evidence for Aggression Towards Non-kin in the Ambrosia Beetle Xyleborinus Saxesenii.
  MELET, Antoine; LEIBOLD, Viesturs; SCHMITT, Thomas & BIEDERMANN, Peter
  
• Know When You Are Too Many: Density-Dependent Release of Pheromones During Host Colonisation by the European Spruce Bark Beetle, Ips typographus (L.). Journal of Chemical Ecology, 49(11-12), 652-665.
  Frühbrodt, Tobias; Du, Baoguo; Delb, Horst; Burzlaff, Tim; Kreuzwieser, Jürgen & Biedermann, Peter H. W.
  
• Verbenone—the universal bark beetle repellent? Its origin, effects, and ecological roles. Journal of Pest Science, 97(1), 35-71.
  Frühbrodt, Tobias; Schebeck, Martin; Andersson, Martin N.; Holighaus, Gerrit; Kreuzwieser, Jürgen; Burzlaff, Tim; Delb, Horst & Biedermann, Peter H. W.
  
• Volatiles of fungal cultivars act as cues for host-selection in the fungus-farming ambrosia beetle Xylosandrus germanus. Frontiers in Microbiology, 14.
  Gugliuzzo, Antonio; Kreuzwieser, Jürgen; Ranger, Christopher M.; Tropea, Garzia Giovanna; Biondi, Antonio & Biedermann, Peter H. W.