The effect of spatial heterogeneity and parasites on the evolution of host diversity

Both spatial heterogeneity and exploiters (parasites and predators) have been implicated as key ecological factors driving population diversification. However, it is unclear how these factors interact. We addressed this question using the common plant‐colonizing bacterium Pseudomonas fluorescens, which has been shown to diversify rapidly into spatial niche‐specialist genotypes when propagated in laboratory microcosms. Replicate populations were evolved in spatially homogeneous and heterogeneous environments (shaken and static microcosms, respectively) with and without viral parasites (bacteriophage) for approximately 60 bacterial generations. Consistent with previous findings, exploiters reduced diversity in heterogeneous environments by relaxing the intensity of resource competition. By contrast, exploiters increased diversity in homogeneous environments where there was little diversification through resource competition. Competition experiments revealed this increase in diversity to be the result of fitness trade‐offs between exploiter resistance and competitive ability. In both environments, exploiters increased allopatric diversity, presumably as a result of divergent selection for resistance between populations. Phage increased total diversity in homogeneous environments, but had no net effect in heterogeneous environments. Such interactions between key ecological variables need to be considered when addressing diversification and coexistence in future studies.

[1]  E. H. Simpson.  Measurement of Diversity , 1949, Nature.

[2]  Francisco J. Ayala,et al.  Frequency-Dependent Selection , 1974 .

[3]  P. Hedrick,et al.  Genetic Polymorphism in Heterogeneous Environments , 1976 .

[4]  R. Holt.  Predation, apparent competition, and the structure of prey communities. , 1977, Theoretical population biology.

[5]  R. Lenski,et al.  Constraints on the Coevolution of Bacteria and Virulent Phage: A Model, Some Experiments, and Predictions for Natural Communities , 1985, The American Naturalist.

[6]  P. Hedrick.  GENETIC POLYMORPHISM IN HETEROGENEOUS ENVIRONMENTS: A DECADE LATER , 1986 .

[7]  R. Lenski,et al.  Long-Term Experimental Evolution in Escherichia coli. I. Adaptation and Divergence During 2,000 Generations , 1991, The American Naturalist.

[8]  R. Lenski,et al.  Long-term experimental evolution in Escherichia coli , 1991 .

[9]  R. Lenski,et al.  Evidence for multiple adaptive peaks from populations of bacteria evolving in a structured habitat. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[10]  R. Herrmann,et al.  B4 – PHYSICAL AND GENETIC MAPPING , 1995 .

[11]  A physical and genetic map of the , 1996 .

[12]  R. Lande.  Statistics and partitioning of species diversity, and similarity among multiple communities , 1996 .

[13]  J. Travis.  The Significance of Geographical Variation in Species Interactions , 1996, The American Naturalist.

[14]  P. Rainey,et al.  Physical and genetic map of the Pseudomonas fluorescens SBW25 chromosome , 1996, Molecular microbiology.

[15]  Jeffrey A. Walker,et al.  Ecological morphology of lacustrine threespine stickleback Gasterosteus aculeatus L. (Gasterosteidae) body shape , 1997 .

[16]  Michael Travisano,et al.  Adaptive radiation in a heterogeneous environment , 1998, Nature.

[17]  J. Thompson,et al.  Specific Hypotheses on the Geographic Mosaic of Coevolution , 1999, The American Naturalist.

[18]  Graham Bell,et al.  Disturbance and diversity in experimental microcosms , 2000, Nature.

[19]  P. Chesson.  Mechanisms of Maintenance of Species Diversity , 2000 .

[20]  Ulf Dieckmann,et al.  Evolutionary Branching and Sympatric Speciation Caused by Different Types of Ecological Interactions , 2000, The American Naturalist.

[21]  R. Lenski,et al.  Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage , 2000 .

[22]  D. Schluter,et al.  The Ecology of Adaptive Radiation , 2000 .

[23]  P. Abrams.  Character Shifts of Prey Species That Share Predators , 2000, The American Naturalist.

[24]  D. Schluter,et al.  Impacts of trout predation on fitness of sympatric sticklebacks and their hybrids , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[25]  P. Abrams,et al.  The Evolution of Traits Affecting Resource Acquisition and Predator Vulnerability: Character Displacement under Real and Apparent Competition , 2002, The American Naturalist.

[26]  A. Buckling,et al.  The role of parasites in sympatric and allopatric host diversification , 2002, Nature.

[27]  Paul B Rainey,et al.  Antagonistic coevolution between a bacterium and a bacteriophage , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[28]  James P. Grover,et al.  The interaction between predation and competition: a review and synthesis , 2002 .