Evolutionary History and Ecological Processes Shape a Local Multilevel Antagonistic Network

Uncovering the processes that shape the architecture of interaction networks is a major challenge in ecology. Studies have consistently revealed that more closely related taxa tend to show greater overlap in interaction partners, fuelling the idea that interactions are phylogenetically conserved. However, local ecological processes such as exploitative or apparent competition (indirect interactions) might instead cause a decrease in overlap in interacting partners. Because of the taxonomic and geographic coarseness of existing studies, the structuring effect of such processes has been overlooked. Here, we assess the relative importance of phylogeny and ecological processes in a local, highly resolved, four-level antagonistic network. Across all network levels we consistently find that phylogenetic relatedness among resource species is correlated with consumer overlap but that phylogenetic relatedness among consumer species is not or negatively correlated with resource overlap. This pervasive pattern indicates that the antagonistic network has been shaped by both phylogeny on resource range and by exploitative competition limiting resource overlap among closely related consumer species. Intriguingly, the strength of phylogenetic signal varies in a consistent way across the network levels. We discuss the generality of our findings and their implications in a changing world.

[1]  John-Arvid Grytnes,et al.  Niche conservatism as an emerging principle in ecology and conservation biology. , 2010, Ecology letters.

[2]  Jordi Bascompte,et al.  Non-random coextinctions in phylogenetically structured mutualistic networks , 2007, Nature.

[3]  J. Ghazoul Floral diversity and the facilitation of pollination , 2006 .

[4]  D. Tilman Resource Competition between Plankton Algae: An Experimental and Theoretical Approach , 1977 .

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

[6]  Luciano Cagnolo,et al.  Network topology: patterns and mechanisms in plant-herbivore and host-parasitoid food webs. , 2011, The Journal of animal ecology.

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

[8]  Dirk Sanders,et al.  Indirect commensalism promotes persistence of secondary consumer species , 2012, Biology Letters.

[9]  K. Schönrogge,et al.  Host Niches and Defensive Extended Phenotypes Structure Parasitoid Wasp Communities , 2009, PLoS biology.

[10]  Miguel Verdú,et al.  Ecological interactions are evolutionarily conserved across the entire tree of life , 2010, Nature.

[11]  Pamela S Soltis,et al.  Darwin's abominable mystery: Insights from a supertree of the angiosperms , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[12]  A. Ives,et al.  Phylogenetic Analysis of Trophic Associations , 2006, The American Naturalist.

[13]  Jordi Bascompte,et al.  Compartments in a marine food web associated with phylogeny, body mass, and habitat structure. , 2009, Ecology letters.

[14]  Jordi Bascompte,et al.  Structure and Dynamics of Ecological Networks , 2010, Science.

[15]  G. F. Gause,et al.  EXPERIMENTAL ANALYSIS OF VITO VOLTERRA'S MATHEMATICAL THEORY OF THE STRUGGLE FOR EXISTENCE. , 1934, Science.

[16]  D. Sanders,et al.  The loss of indirect interactions leads to cascading extinctions of carnivores. , 2013, Ecology letters.

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

[18]  H Charles J Godfray,et al.  Apparent competition, quantitative food webs, and the structure of phytophagous insect communities. , 2006, Annual review of entomology.

[19]  Rudolf P. Rohr,et al.  Phylogeny versus body size as determinants of food web structure , 2012, Proceedings of the Royal Society B: Biological Sciences.

[20]  David Mouillot,et al.  Phylogenetic Signal in Module Composition and Species Connectivity in Compartmentalized Host-Parasite Networks , 2012, The American Naturalist.

[21]  M. Hassell,et al.  Apparent competition structures ecological assemblages , 1997, Nature.

[22]  J. Whitfield,et al.  Phylogeny and evolution of host-parasitoid interactions in hymenoptera. , 1998, Annual review of entomology.

[23]  L. Harmon,et al.  POOR STATISTICAL PERFORMANCE OF THE MANTEL TEST IN PHYLOGENETIC COMPARATIVE ANALYSES , 2010, Evolution; international journal of organic evolution.

[24]  H. Godfray,et al.  Food web structure of three guilds of natural enemies: predators, parasitoids and pathogens of aphids. , 2008, The Journal of animal ecology.

[25]  Jean-Pierre Gabriel,et al.  Phylogenetic constraints and adaptation explain food-web structure , 2004, Nature.

[26]  Corinne Vacher,et al.  Architecture of an Antagonistic Tree/Fungus Network: The Asymmetric Influence of Past Evolutionary History , 2008, PloS one.

[27]  Kimberly S. Sheldon,et al.  Climate change and community disassembly: impacts of warming on tropical and temperate montane community structure. , 2011, Ecology letters.

[28]  F. Jiguet,et al.  Differences in the climatic debts of birds and butterflies at a continental scale , 2012 .

[29]  J. Losos Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. , 2008, Ecology letters.

[30]  Kimberly S. Sheldon,et al.  On a collision course: competition and dispersal differences create no-analogue communities and cause extinctions during climate change , 2012, Proceedings of the Royal Society B: Biological Sciences.

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

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

[33]  J. Felsenstein CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[34]  F. Veen,et al.  Body Size, Life History and the Structure of Host–Parasitoid Networks , 2011 .

[35]  Campbell O. Webb,et al.  Phylogenetic signal in plant pathogen–host range , 2007, Proceedings of the National Academy of Sciences.

[36]  Owen L Petchey,et al.  Size, foraging, and food web structure , 2008, Proceedings of the National Academy of Sciences.

[37]  L. Bersier,et al.  The signature of phylogenetic constraints on food-web structure , 2008 .

[38]  D. Penny The comparative method in evolutionary biology , 1992 .

[39]  H. Charles J. Godfray,et al.  Experimental evidence for apparent competition in a tropical forest food web , 2004, Nature.

[40]  L. Slobodkin,et al.  Community Structure, Population Control, and Competition , 1960, The American Naturalist.

[41]  J. Wootton,et al.  The Nature and Consequences of Indirect Effects in Ecological Communities , 1994 .

[42]  M. E. Huigens,et al.  Male-derived butterfly anti-aphrodisiac mediates induced indirect plant defense , 2008, Proceedings of the National Academy of Sciences.

[43]  J. R. Ott,et al.  Interspecific interactions in phytophagous insects : competition reexamined and resurrected , 1995 .

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

[45]  D. Tyteca,et al.  Analysis of network architecture reveals phylogenetic constraints on mycorrhizal specificity in the genus Orchis (Orchidaceae). , 2011, The New phytologist.

[46]  R. Fisher Statistical methods for research workers , 1927, Protoplasma.