A SLOWLY EVOLVING HOST MOVES FIRST IN SYMBIOTIC INTERACTIONS

Symbiotic relationships, both parasitic and mutualistic, are ubiquitous in nature. Understanding how these symbioses evolve, from bacteria and their phages to humans and our gut microflora, is crucial in understanding how life operates. Often, symbioses consist of a slowly evolving host species with each host only interacting with its own subpopulation of symbionts. The Red Queen hypothesis describes coevolutionary relationships as constant arms races with each species rushing to evolve an advantage over the other, suggesting that faster evolution is favored. Here, we use a simple game theoretic model of host–symbiont coevolution that includes population structure to show that if the symbionts evolve much faster than the host, the equilibrium distribution is the same as it would be if it were a sequential game where the host moves first against its symbionts. For the slowly evolving host, this will prove to be advantageous in mutualisms and a handicap in antagonisms. The result follows from rapid symbiont adaptation to its host and is robust to changes in the parameters, even generalizing to continuous and multiplayer games. Our findings provide insight into a wide range of symbiotic phenomena and help to unify the field of coevolutionary theory.

[1]  Steven J. Brams,et al.  Threat Power in Sequential Games , 1984 .

[2]  A. W. F. Edwards,et al.  The statistical processes of evolutionary theory , 1963 .

[3]  L. V. Valen,et al.  A new evolutionary law , 1973 .

[4]  M. Nowak,et al.  Evolutionary dynamics in structured populations , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[5]  U. Mueller,et al.  The evolution of mutualisms: exploring the paths between conflict and cooperation. , 1999, Trends in ecology & evolution.

[6]  M. Doebeli,et al.  The evolution of interspecific mutualisms. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Sam P. Brown,et al.  Within-Host Competition Drives Selection for the Capsule Virulence Determinant of Streptococcus pneumoniae , 2010, Current Biology.

[8]  Alexander Vologodskii,et al.  Sequence dependence of DNA bending rigidity , 2010, Proceedings of the National Academy of Sciences.

[9]  J. Krebs,et al.  Arms races between and within species , 1979, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[10]  C. Hauert,et al.  The Evolutionary Origin of Cooperators and Defectors , 2004, Science.

[11]  C. Hauert,et al.  Models of cooperation based on the Prisoner's Dilemma and the Snowdrift game , 2005 .

[12]  A. Thompson Habitat and mutualism affect the distribution and abundance of a shrimp-associated goby , 2004 .

[13]  D. J. Funk,et al.  Mutation Exposed: A Neutral Explanation for Extreme Base Composition of an Endosymbiont Genome , 2004, Journal of Molecular Evolution.

[14]  Matthias E. Futschik,et al.  Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution , 2007, Nature.

[15]  A. Neish The gut microflora and intestinal epithelial cells: a continuing dialogue. , 2002, Microbes and infection.

[16]  Douglas W. Yu,et al.  Selection for protection in an ant–plant mutualism: host sanctions, host modularity, and the principal–agent game , 2006, Proceedings of the Royal Society B: Biological Sciences.

[17]  J. Bull,et al.  Short-sighted evolution and the virulence of pathogenic microorganisms. , 1994, Trends in microbiology.

[18]  E. Leigh The evolution of mutualism , 2010, Journal of evolutionary biology.

[19]  C. Pál,et al.  Coevolution with viruses drives the evolution of bacterial mutation rates , 2007, Nature.

[20]  N. Pierce,et al.  The selective advantage of attendant ants for the larvae of a lycaenid butterfly, Glaucopsyche lygdamus , 1986 .

[21]  A. van Oudenaarden,et al.  Snowdrift game dynamics and facultative cheating in yeast , 2009, Nature.

[22]  Carl T. Bergstrom,et al.  The Red King effect: When the slowest runner wins the coevolutionary race , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Eduardo P C Rocha,et al.  Base composition bias might result from competition for metabolic resources. , 2002, Trends in genetics : TIG.

[24]  K R Foster,et al.  A general model for the evolution of mutualisms , 2006, Journal of evolutionary biology.

[25]  M. Nowak,et al.  Evolutionary Dynamics of Biological Games , 2004, Science.

[26]  S. Nechaev,et al.  The elusive object of desire--interactions of bacteriophages and their hosts. , 2008, Current opinion in microbiology.

[27]  D. DeAngelis,et al.  Evolutionary stability of mutualism: interspecific population regulation as an evolutionarily stable strategy , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[28]  Paul Baumann,et al.  Faster evolutionary rates in endosymbiotic bacteria than in cospeciating insect hosts , 2004, Journal of Molecular Evolution.

[29]  J. M. Smith,et al.  The Logic of Animal Conflict , 1973, Nature.

[30]  Marcus Frean,et al.  Adaptation and enslavement in endosymbiont-host associations. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[31]  M. Rausher,et al.  Two modes of host–enemy coevolution , 2001, Population Ecology.

[32]  M. Nowak Evolutionary Dynamics: Exploring the Equations of Life , 2006 .

[33]  D. Koller,et al.  The complexity of two-person zero-sum games in extensive form , 1992 .

[34]  W. Hamilton,et al.  The evolution of cooperation. , 1984, Science.

[35]  P. Kilmarx,et al.  Global epidemiology of HIV , 2009, Current opinion in HIV and AIDS.

[36]  J. Bull,et al.  Distinguishing mechanisms for the evolution of co-operation. , 1991, Journal of theoretical biology.

[37]  M. Hattori,et al.  Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS , 2000, Nature.

[38]  R. Gomulkiewicz,et al.  Gene flow and geographically structured coevolution , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.