Effects of evolutionary changes in prey use on the relationship between food web complexity and stability

The relationship between food web complexity and stability has been the subject of a long-standing debate in ecology. Although rapid changes in the food web structure through adaptive foraging behavior can confer stability to complex food webs, as reported by Kondoh (Science 299:1388–1391, 2003), the exact mechanisms behind this adaptation have not been specified in previous studies; thus, the applicability of such predictions to real ecosystems remains unclear. One mechanism of adaptive foraging is evolutionary change in genetically determined prey use. We constructed individual-based models of evolution of prey use by predators assuming explicit population genetics processes, and examined how this evolution affects the stability (i.e., the proportion of species that persist) of the food web and whether the complexity of the food web increased the stability of the prey–predator system. The analysis showed that the stability of food webs decreased with increasing complexity regardless of evolution of prey use by predators. The effects of evolution on stability differed depending on the assumptions made regarding genetic control of prey use. The probabilities of species extinctions were associated with the establishment or loss of trophic interactions via evolution of the predator, indicating a clear link between structural changes in the food web and community stability.

[1]  R. Macarthur.  Fluctuations of Animal Populations and a Measure of Community Stability , 1955 .

[2]  ROBERT M. MAY,et al.  Will a Large Complex System be Stable? , 1972, Nature.

[3]  T. Smith,et al.  Disruptive selection and the genetic basis of bill size polymorphism in the African finch Pyrenestes , 1993, Nature.

[4]  Caldarelli,et al.  Modelling Coevolution in Multispecies Communities. , 1998, Journal of theoretical biology.

[5]  A. Ives,et al.  Stability and variability in competitive communities. , 1999, Science.

[6]  J. Feder,et al.  Natural selection and sympatric divergence in the apple maggot Rhagoletis pomonella , 2000, Nature.

[7]  P. Abrams.  The Evolution of Predator-Prey Interactions: Theory and Evidence , 2000 .

[8]  K. McCann.  The diversity–stability debate , 2000, Nature.

[9]  D. Bolnick.  Intraspecific competition favours niche width expansion in Drosophila melanogaster , 2001, Nature.

[10]  M. Egas,et al.  Adaptive learning of host preference in a herbivorous arthropod , 2001 .

[11]  S. Hubbell,et al.  The unified neutral theory of biodiversity and biogeography at age ten. , 2011, Trends in ecology & evolution.

[12]  Anurag A. Agrawal,et al.  Phenotypic Plasticity in the Interactions and Evolution of Species , 2001, Science.

[13]  Ricard V. Solé,et al.  Complexity and fragility in ecological networks , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[14]  L. Vitt,et al.  Food Web Laws or Niche Theory? Six Independent Empirical Tests , 2001, The American Naturalist.

[15]  David J. Hawthorne,et al.  Genetic linkage of ecological specialization and reproductive isolation in pea aphids , 2001, Nature.

[16]  D. J. Funk,et al.  GEOGRAPHIC VARIATION IN HOST SPECIFICITY REVEALS HOST RANGE EVOLUTION IN UROLEUCON AMBROSIAE APHIDS , 2001 .

[17]  H. Mooney,et al.  The evolutionary impact of invasive species , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[18]  B. Drossel,et al.  The influence of predator--prey population dynamics on the long-term evolution of food web structure. , 2000, Journal of theoretical biology.

[19]  K. Christensen,et al.  Tangled nature: a model of evolutionary ecology. , 2001, Journal of theoretical biology.

[20]  V. Jansen,et al.  Variability in interaction strength and implications for biodiversity , 2002 .

[21]  H. F. Nijhout,et al.  Stability in Real Food Webs: Weak Links in Long Loops , 2002 .

[22]  R. Kassen.  The experimental evolution of specialists, generalists, and the maintenance of diversity , 2002 .

[23]  J. Montoya,et al.  Small world patterns in food webs. , 2002, Journal of theoretical biology.

[24]  Neo D. Martinez,et al.  Network structure and biodiversity loss in food webs: robustness increases with connectance , 2002, Ecology Letters.

[25]  A. Dixon,et al.  Costs and benefits of prey specialization in a generalist insect predator , 2002 .

[26]  D. Mason,et al.  Compartments revealed in food-web structure , 2003, Nature.

[27]  Neo D. Martinez,et al.  Comment on "Foraging Adaptation and the Relationship Between Food-Web Complexity and Stability" , 2003, Science.

[28]  V. Jansen,et al.  Complexity and stability revisited , 2003 .

[29]  Michio Kondoh,et al.  Response to Comment on "Foraging Adaptation and the Relationship Between Food-Web Complexity and Stability" , 2003, Science.

[30]  David Waxmany,et al.  20 Questions on Adaptive Dynamics: A Target Review , 2004 .

[31]  J. Lambrinos.  HOW INTERACTIONS BETWEEN ECOLOGY AND EVOLUTION INFLUENCE CONTEMPORARY INVASION DYNAMICS , 2004 .

[32]  M. Emmerson,et al.  Predator–prey body size, interaction strength and the stability of a real food web , 2004 .

[33]  D. Reznick,et al.  The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution , 2004, Genetica.

[34]  Christopher Quince,et al.  Topological structure and interaction strengths in model food webs , 2004, q-bio/0402014.

[35]  Barbara Drossel,et al.  The impact of non-linear functional responses on the long-term evolution of food web structure , 2004 .

[36]  M. Doebeli,et al.  GENETIC CORRELATIONS AND THE COEVOLUTIONARY DYNAMICS OF THREE-SPECIES SYSTEMS , 2004 .

[37]  Barbara Drossel,et al.  The impact of nonlinear functional responses on the long-term evolution of food web structure. , 2004, Journal of theoretical biology.

[38]  Jane Memmott,et al.  Tolerance of pollination networks to species extinctions , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[39]  M. Doebeli,et al.  GENETIC CORRELATIONS AND THE COEVOLUTIONARY DYNAMICS OF THREE‐SPECIES SYSTEMS , 2004, Evolution; international journal of organic evolution.

[40]  Hiroyuki Matsuda,et al.  Effects of predator-specific defence on biodiversity and community complexity in two-trophic-level communities , 2005, Evolutionary Ecology.

[41]  N. Yamamura,et al.  EFFECTS OF DEFENSE EVOLUTION AND DIET CHOICE ON POPULATION DYNAMICS IN A ONE‐PREDATOR–TWO‐PREY SYSTEM , 2005 .

[42]  Michel Loreau,et al.  Trophic Interactions and the Relationship between Species Diversity and Ecosystem Stability , 2005, The American Naturalist.

[43]  Mathew A. Leibold,et al.  Metacommunities: Spatial Dynamics and Ecological Communities , 2005 .

[44]  J. Duffy,et al.  Ecosystem consequences of diversity depend on food chain length in estuarine vegetation , 2005 .

[45]  P. A. Rikvold,et al.  Effects of correlated interactions in a biological coevolution model with individual-based dynamics , 2005, q-bio/0507040.

[46]  Henrik Jeldtoft Jensen,et al.  Network properties, species abundance and evolution in a model of evolutionary ecology. , 2003, Journal of theoretical biology.

[47]  R. Solé,et al.  Ecological networks and their fragility , 2006, Nature.

[48]  Henrik Jeldtoft Jensen,et al.  Correlation, selection and the evolution of species networks , 2006, q-bio/0608004.

[49]  M. Kawata,et al.  A genetically explicit model of speciation by sensory drive within a continuous population in aquatic environments , 2007, BMC Evolutionary Biology.

[50]  M. Pascual,et al.  Ecological networks : Linking structure to dynamics in food webs , 2006 .

[51]  Jordi Bascompte,et al.  Asymmetric Coevolutionary Networks Facilitate Biodiversity Maintenance , 2006, Science.

[52]  M. Kinnison,et al.  Eco-evolutionary conservation biology: contemporary evolution and the dynamics of persistence , 2007 .

[53]  C. McBride,et al.  Rapid evolution of smell and taste receptor genes during host specialization in Drosophila sechellia , 2007, Proceedings of the National Academy of Sciences.

[54]  Michel Loreau,et al.  Eco‐evolutionary dynamics of communities and ecosystems , 2007 .

[55]  I. Ohshima.  Host race formation in the leaf-mining moth Acrocercops transecta (Lepidoptera: Gracillariidae) , 2007 .

[56]  J. Stinchcombe,et al.  An emerging synthesis between community ecology and evolutionary biology. , 2007, Trends in ecology & evolution.

[57]  P. A. Rikvold,et al.  Self-optimization, community stability, and fluctuations in two individual-based models of biological coevolution , 2005, Journal of mathematical biology.

[58]  S. Carpenter,et al.  Stability and Diversity of Ecosystems , 2007, Science.

[59]  Barbara Drossel,et al.  Relation between complexity and stability in food webs with adaptive behavior. , 2007, Journal of theoretical biology.

[60]  R. Ricklefs.  History and Diversity: Explorations at the Intersection of Ecology and Evolution , 2007, The American Naturalist.

[61]  Michel Loreau,et al.  The functional role of biodiversity in ecosystems: incorporating trophic complexity. , 2007, Ecology letters.

[62]  G. Bell,et al.  The evolution of trophic structure , 2007, Heredity.

[63]  Josep L. Garcia-Domingo,et al.  Food-web complexity emerging from ecological dynamics on adaptive networks. , 2007, Journal of theoretical biology.

[64]  A. Rossberg,et al.  The top-down mechanism for body-mass-abundance scaling. , 2008, Ecology.

[65]  Jean-Pierre Gabriel,et al.  Complexity in quantitative food webs. , 2009, Ecology.

[66]  Lin Jiang,et al.  Different Effects of Species Diversity on Temporal Stability in Single‐Trophic and Multitrophic Communities , 2009, The American Naturalist.