Evolutionary dynamics of mutualists during territorial expansion

• Applicant: Dr. Melanie Mueller
• Subject Area: Bioinformatics and Theoretical Biology
• Term: from 2011 to 2014
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 201655341

• Final Report Year: 2015

Final Report Abstract

Spatial expansion of mutualists. Mutualism is an interaction between two species that is beneficial for both partners. Mutualisms are widespread and often critical parts of ecosystems, for example trees and their mutualistic root fungi, or flowering plants and their insect pollinators like bees or butterflies. After mutualisms form for the first time, or when environmental conditions change, the mutualistic partners have to spread together to new territories. Several major events in evolutionary history include the spatial expansion of mutualists. For example, the first conquest of land by plants may have been made possible by their mutualist association with fungi, and newly evolved flowering plants spread with their pollen-dispersing insects. More recently, the invasion of pine trees in the Southern hemisphere required fungal mutualists. On much smaller scales, microbes that grow in biofilms on surfaces often exhibit mutualistic interactions, such as bacteria growing on teeth, or fungi growing on the inside of tubings. Our approach. In this project, we investigated the effect of spatial expansion on mutualistic species, using a combination of theoretical and experimental approaches. For the theoretical modeling we used approaches from statistical physics and population dynamics. Our experimental model system was a pair of yeast strains that feed each other essential nutrients while spreading on the surface of a Petri dish. This model system has the advantage of short generation times and tightly controlled growth conditions, but is also close to ‘real-world’ microbial biofilms. Spatial expansion impedes mutualism. Overall, we find that spatial expansion poses a challenge for mutualists. During the expansion, the first few individuals to arrive in the new territory are likely to be the ancestors, or founders, of the later populations in this area. This founder effect produces regions which are populated exclusively, or to a large majority, by only one of the two partners. This makes the mutualistic interaction less efficient and therefore less beneficial, leading to impeded proliferation and potentially even loss of mutualism. More quantitatively, we calculate how strong mutualism has to be in order to ‘survive’ a spatial expansion. For the case of successfully expanding strong mutualists we characterize the spatial pattern and expansion velocity of the partners. This analysis helps to understand what happens during the territorial expansion of mutualists. It could also be used to infer information about the mutualistic interaction from observed spatial patterns during of after the territorial expansion of mutualistic species. Consequences for natural mutualistic systems. Our observations imply that spatial expansions, like those caused by climate shifts, could destroy, or at least strongly impede, existing mutualisms. In order to survive spatial expansions, mutualistic interactions must be sustained by strong mutualistic benefits, or be able to rely on mechanisms that ensure coordinated dispersal of the mutualistic partners. This constraint may have shaped the evolution of mutualisms in nature. It allows for only the spread of very beneficial mutualisms, e.g., the invasion of land by plants with mycorrhizal fungi and flowering plants with pollen dispersing insects. It can also lead to the evolution of additional mechanisms for coordinated dispersal, such as physical attachment of the partners in endosymbionts and lichens.

Publications

• Selective sweeps in growing microbial colonies, Phys. Biol. 9, 026008 (2012)
  K.S. Korolev, M.J.I. Müller, N. Karahan, A.W. Murray, O. Hallatschek, and D.R. Nelson
  
• Spatial population expansion promotes the evolution of cooperation in an experimental Prisoner’s Dilemma, Curr. Biol. 23, 919 (2013)
  J.D. van Dyken, M.J.I. Müller, K.M. Mack, M.D. Desai
  
• Genetic drift opposes mutualism during spatial population expansion, Proc. Natl. Acad. Sci. USA 111, 1037-1042 (2014)
  M.J.I. Müller, B.I. Neugeboren, D.R. Nelson, and A.W. Murray