COEVOLUTION AND THE ARCHITECTURE OF MUTUALISTIC NETWORKS

Although coevolution is widely recognized as an important evolutionary process for pairs of reciprocally specialized species, its importance within species‐rich communities of generalized species has been questioned. Here we develop and analyze mathematical models of mutualistic communities, such as those between plants and pollinators or plants and seed‐dispersers to evaluate the importance of coevolutionary selection within complex communities. Our analyses reveal that coevolutionary selection can drive significant changes in trait distributions with important consequences for the network structure of mutualistic communities. One such consequence is greater connectance caused by an almost invariable increase in the rate of mutualistic interaction within the community. Another important consequence is altered patterns of nestedness. Specifically, interactions mediated by a mechanism of phenotype matching tend to be antinested when coevolutionary selection is weak and even more strongly antinested as increasing coevolutionary selection favors the emergence of reciprocal specialization. In contrast, interactions mediated by a mechanism of phenotype differences tend to be nested when coevolutionary selection is weak, but less nested as increasing coevolutionary selection favors greater levels of generalization in both plants and animals. Taken together, our results show that coevolutionary selection can be an important force within mutualistic communities, driving changes in trait distributions, interaction rates, and even network structure.

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

[2]  R. Plevin,et al.  Approximate Bayesian Computation in Evolution and Ecology , 2011 .

[3]  S. Gandon,et al.  Interactions between Genetic Drift, Gene Flow, and Selection Mosaics Drive Parasite Local Adaptation , 2008, The American Naturalist.

[4]  M. Wade.  The co-evolutionary genetics of ecological communities , 2007, Nature Reviews Genetics.

[5]  P. Klinkhamer,et al.  Size constraints and flower abundance determine the number of interactions in a plant /flower visitor web , 2006 .

[6]  Luciano Cagnolo,et al.  Evaluating multiple determinants of the structure of plant-animal mutualistic networks. , 2009, Ecology.

[7]  A. Ellis,et al.  Predictable patterns of trait mismatches between interacting plants and insects , 2010, BMC Evolutionary Biology.

[8]  Daniel B. Stouffer,et al.  Nestedness versus modularity in ecological networks: two sides of the same coin? , 2010, The Journal of animal ecology.

[9]  Jordi Bascompte,et al.  Plant-Animal Mutualistic Networks: The Architecture of Biodiversity , 2007 .

[10]  S. Otto,et al.  Species Interactions and the Evolution of Sex , 2004, Science.

[11]  B. J. Borrell.  Scaling of Nectar Foraging in Orchid Bees , 2007, The American Naturalist.

[12]  R. Lande.  NATURAL SELECTION AND RANDOM GENETIC DRIFT IN PHENOTYPIC EVOLUTION , 1976, Evolution; international journal of organic evolution.

[13]  Steiner,et al.  Generalization versus specialization in plant pollination systems. , 2000, Trends in ecology & evolution.

[14]  Salvatore J. Agosta,et al.  Body size distributions of large Costa Rican dry forest moths and the underlying relationship between plant and pollinator morphology , 2005 .

[15]  M. Wade.  COMMUNITY GENETICS AND SPECIES INTERACTIONS , 2003 .

[16]  Erik E Osnas,et al.  Host Sex and Local Adaptation by Parasites in a Snail‐Trematode Interaction , 2004, The American Naturalist.

[17]  S. Gavrilets,et al.  MULTILOCUS GENETICS AND THE COEVOLUTION OF QUANTITATIVE TRAITS , 2006, Evolution; international journal of organic evolution.

[18]  Frank Lambert,et al.  Fig-eating by birds in a Malaysian lowland rain forest , 1989, Journal of Tropical Ecology.

[19]  M. Rausher,et al.  Diffuse Selection on Resistance to Deer Herbivory in the Ivyleaf Morning Glory, Ipomoea hederacea , 2001, The American Naturalist.

[20]  Paulo R. Guimarães,et al.  Interaction Intimacy Affects Structure and Coevolutionary Dynamics in Mutualistic Networks , 2007, Current Biology.

[21]  S. Nuismer,et al.  ANTAGONISTIC COEVOLUTION MEDIATED BY PHENOTYPIC DIFFERENCES BETWEEN QUANTITATIVE TRAITS , 2007, Evolution; international journal of organic evolution.

[22]  Mark D. Rausher,et al.  Evolution of Plant Resistance to Multiple Herbivores: Quantifying Diffuse Coevolution , 1997, The American Naturalist.

[23]  Réka Albert,et al.  A network model for plant–pollinator community assembly , 2010, Proceedings of the National Academy of Sciences.

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

[25]  S. Gavrilets,et al.  Coevolutionary chase on exploiter-victim systems with polygenic characters. , 1997, Journal of theoretical biology.

[26]  Jordi Bascompte,et al.  Missing and forbidden links in mutualistic networks , 2011, Proceedings of the Royal Society B: Biological Sciences.

[27]  J. Bascompte,et al.  Effects of phenotypic complementarity and phylogeny on the nested structure of mutualistic networks , 2007 .

[28]  G. Bertorelle,et al.  ABC as a flexible framework to estimate demography over space and time: some cons, many pros , 2010, Molecular ecology.

[29]  J. Bascompte,et al.  Invariant properties in coevolutionary networks of plant-animal interactions , 2002 .

[30]  C. Lively.  A review of Red Queen models for the persistence of obligate sexual reproduction. , 2010, The Journal of heredity.

[31]  D. Levey.  Seed Size and Fruit-Handling Techniques of Avian Frugivores , 1987, The American Naturalist.

[32]  R. Lande,et al.  Models of Coevolution and Speciation in Plants and Their Pollinators , 1984, The American Naturalist.

[33]  Nicolas Loeuille,et al.  The ecological and evolutionary implications of merging different types of networks. , 2011, Ecology letters.

[34]  P. Asprelli,et al.  THE GEOGRAPHIC MOSAIC OF COEVOLUTION , 2007 .

[35]  Luis Santamaría,et al.  Linkage Rules for Plant–Pollinator Networks: Trait Complementarity or Exploitation Barriers? , 2007, PLoS biology.

[36]  Mark D. Rausher,et al.  Interactions between Herbivorous Insects and Plant-Insect Coevolution , 1994, The American Naturalist.

[37]  THE COEVOLUTIONARY DYNAMICS OF ANTAGONISTIC INTERACTIONS MEDIATED BY QUANTITATIVE TRAITS WITH EVOLVING VARIANCES , 2005, Evolution; international journal of organic evolution.

[38]  D. Inouye.  The effect of proboscis and corolla tube lengths on patterns and rates of flower visitation by bumblebees , 1980, Oecologia.

[39]  A. Agrawal.  Similarity Selection and the Evolution of Sex: Revisiting the Red Queen , 2006, PLoS biology.

[40]  Jochen Fründ,et al.  What do interaction network metrics tell us about specialization and biological traits? , 2008, Ecology.

[41]  S. Otto,et al.  Host-parasite interactions and the evolution of ploidy. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[42]  M. Salathé,et al.  The state of affairs in the kingdom of the Red Queen. , 2008, Trends in ecology & evolution.

[43]  S. Johnson,et al.  Geographical covariation and local convergence of flower depth in a guild of fly-pollinated plants. , 2009, The New phytologist.

[44]  R. Gomulkiewicz,et al.  When Is Correlation Coevolution? , 2010, The American Naturalist.

[45]  O. François,et al.  Approximate Bayesian Computation (ABC) in practice. , 2010, Trends in ecology & evolution.

[46]  Alfonso Valiente-Banuet,et al.  The relative contribution of abundance and phylogeny to the structure of plant facilitation networks , 2011 .

[47]  S. Otto,et al.  When do host-parasite interactions drive the evolution of non-random mating? , 2008, Ecology letters.

[48]  P. Jordano,et al.  The Functional Consequences of Mutualistic Network Architecture , 2011, PloS one.

[49]  M. Rausher.  Genetic analysis of coevolution between plants and their natural enemies. , 1996, Trends in genetics : TIG.

[50]  Ricard V. Solé,et al.  On nestedness in ecological networks , 2010 .

[51]  S. Gandon,et al.  Local adaptation and gene-for-gene coevolution in a metapopulation model , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[52]  Carlos J. Melián,et al.  The nested assembly of plant–animal mutualistic networks , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[53]  Marcelo Tabarelli,et al.  Tree species impoverishment and the future flora of the Atlantic forest of northeast Brazil , 2000, Nature.

[54]  Jordi Bascompte,et al.  A neutral‐niche theory of nestedness in mutualistic networks , 2008 .

[55]  James Rosindell,et al.  Unified neutral theory of biodiversity and biogeography , 2010, Scholarpedia.

[56]  Werner Ulrich,et al.  A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement , 2008 .

[57]  Rebecca E. Irwin,et al.  Ecological and Evolutionary Consequences of Multispecies Plant-Animal Interactions , 2004 .

[58]  J. Burdon,et al.  Coevolution at multiple spatial scales: Linum marginale–Melampsora lini – from the individual to the species , 2000, Evolutionary Ecology.

[59]  Michele R. Dudash,et al.  Pollination Syndromes and Floral Specialization , 2004 .

[60]  Pedro Jordano,et al.  Evolution and Coevolution in Mutualistic Networks , 2022 .

[61]  P. Klinkhamer,et al.  Asymmetric specialization and extinction risk in plant–flower visitor webs: a matter of morphology or abundance? , 2007, Oecologia.