Covariation and phenotypic integration in chemical communication displays: biosynthetic constraints and eco-evolutionary implications.

Chemical communication is ubiquitous. The identification of conserved structural elements in visual and acoustic communication is well established, but comparable information on chemical communication displays (CCDs) is lacking. We assessed the phenotypic integration of CCDs in a meta-analysis to characterize patterns of covariation in CCDs and identified functional or biosynthetically constrained modules. Poorly integrated plant CCDs (i.e. low covariation between scent compounds) support the notion that plants often utilize one or few key compounds to repel antagonists or to attract pollinators and enemies of herbivores. Animal CCDs (mostly insect pheromones) were usually more integrated than those of plants (i.e. stronger covariation), suggesting that animals communicate via fixed proportions among compounds. Both plant and animal CCDs were composed of modules, which are groups of strongly covarying compounds. Biosynthetic similarity of compounds revealed biosynthetic constraints in the covariation patterns of plant CCDs. We provide a novel perspective on chemical communication and a basis for future investigations on structural properties of CCDs. This will facilitate identifying modules and biosynthetic constraints that may affect the outcome of selection and thus provide a predictive framework for evolutionary trajectories of CCDs in plants and animals.

[1]  J. Gershenzon,et al.  The Chemical Diversity of Floral Scent , 2020, Biology of Plant Volatiles.

[2]  Adam C. Wilkinson,et al.  Branched-chain amino acid metabolism in cancer , 2017, Current opinion in clinical nutrition and metabolic care.

[3]  R. Junker,et al.  Time-invariant differences between plant individuals in interactions with arthropods correlate with intraspecific variation in plant phenology, morphology and floral scent. , 2016, The New phytologist.

[4]  D. Heckel,et al.  The Genetic Basis of Pheromone Evolution in Moths. , 2016, Annual review of entomology.

[5]  F. Menzel,et al.  Ecology and Evolution of Communication in Social Insects , 2016, Cell.

[6]  M. Erb,et al.  Herbivore intoxication as a potential primary function of an inducible volatile plant signal , 2016 .

[7]  S. Levinson.  Turn-taking in Human Communication – Origins and Implications for Language Processing , 2016, Trends in Cognitive Sciences.

[8]  R. Junker.  Multifunctional and Diverse Floral Scents Mediate Biotic Interactions Embedded in Communities , 2016 .

[9]  Stacey D. Smith.  Pleiotropy and the evolution of floral integration. , 2016, The New phytologist.

[10]  G. Ruxton,et al.  Signal Diversity, Sexual Selection, and Speciation , 2015 .

[11]  Matthew R. Wilkins,et al.  Multimodal signalling in the North American barn swallow: a phenotype network approach , 2015, Proceedings of the Royal Society B: Biological Sciences.

[12]  T. Blankers,et al.  Phenotypic variation and covariation indicate high evolvability of acoustic communication in crickets , 2015, Journal of evolutionary biology.

[13]  William D. Pearse,et al.  Pez: Phylogenetics for the Environmental Sciences , 2015, Bioinform..

[14]  S. Dötterl,et al.  Diacetin, a reliable cue and private communication channel in a specialized pollination system , 2015, Scientific Reports.

[15]  C. E. Allen,et al.  Selection on male sex pheromone composition contributes to butterfly reproductive isolation , 2015, Proceedings of the Royal Society B: Biological Sciences.

[16]  N. Blüthgen,et al.  Functional and phylogenetic diversity of plant communities differently affect the structure of flower-visitor interactions and reveal convergences in floral traits , 2015, Evolutionary Ecology.

[17]  M. Skidmore,et al.  Corrigendum: A microbial ecosystem beneath the West Antarctic ice sheet , 2014, Nature.

[18]  David C. Tank,et al.  Erratum: Three keys to the radiation of angiosperms into freezing environments (Nature (2014) 506 (89-92) (Doi:10.1038/nature12872)) , 2014 .

[19]  T. Münkemüller,et al.  Identifying the signal of environmental filtering and competition in invasion patterns – a contest of approaches from community ecology , 2014 .

[20]  M. Reichelt,et al.  Herbivore-induced volatile emission in black poplar: regulation and role in attracting herbivore enemies. , 2014, Plant, cell & environment.

[21]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[22]  A. Classen,et al.  Within-population variability in a moth sex pheromone blend: genetic basis and behavioural consequences , 2014, Proceedings of the Royal Society B: Biological Sciences.

[23]  David C. Tank,et al.  Three keys to the radiation of angiosperms into freezing environments , 2013, Nature.

[24]  T. Wyatt.  Introduction to Chemical Signaling in Vertebrates and Invertebrates , 2014 .

[25]  C. Mucignat-Caretta.  Introduction to Chemical Signaling in Vertebrates and Invertebrates -- Neurobiology of Chemical Communication , 2014 .

[26]  D. Bates,et al.  fitting linear mixed effects models using lme 4 arxiv , 2014 .

[27]  K. Mori,et al.  Elucidating Structure-Bioactivity Relationships of Methyl-Branched Alkanes in the Contact Sex Pheromone of the Parasitic Wasp Lariophagus distinguendus , 2013, Insects.

[28]  S. Johnson,et al.  Pollinator-mediated evolution of floral signals. , 2013, Trends in ecology & evolution.

[29]  R. Borges,et al.  Diel Variation in Fig Volatiles Across Syconium Development: Making Sense of Scents , 2013, Journal of Chemical Ecology.

[30]  Natalia Dudareva,et al.  Biosynthesis, function and metabolic engineering of plant volatile organic compounds. , 2013, The New phytologist.

[31]  Charles E. Taylor,et al.  Structural Design Principles of Complex Bird Songs: A Network-Based Approach , 2012, PloS one.

[32]  R. Raguso,et al.  Phenotypic selection to increase floral scent emission, but not flower size or colour in bee-pollinated Penstemon digitalis. , 2012, The New phytologist.

[33]  Liam J. Revell,et al.  phytools: an R package for phylogenetic comparative biology (and other things) , 2012 .

[34]  J. Gershenzon,et al.  Floral Odor Bouquet Loses its Ant Repellent Properties After Inhibition of Terpene Biosynthesis , 2011, Journal of Chemical Ecology.

[35]  J. Pickett,et al.  Perception of plant volatile blends by herbivorous insects--finding the right mix. , 2011, Phytochemistry.

[36]  T. Bukovinszky,et al.  Smelling the Wood from the Trees: Non-Linear Parasitoid Responses to Volatile Attractants Produced by Wild and Cultivated Cabbage , 2011, Journal of Chemical Ecology.

[37]  G. Kaiser.  Functional and Phylogenetic Diversity in Marine and Aquatic Birds , 2011 .

[38]  P. Jordano,et al.  Colour, design and reward: phenotypic integration of fleshy fruit displays , 2011, Journal of evolutionary biology.

[39]  H. Miziorko.  Enzymes of the mevalonate pathway of isoprenoid biosynthesis. , 2011, Archives of biochemistry and biophysics.

[40]  T. Schmitt,et al.  The origin and dynamic evolution of chemical information transfer , 2011, Proceedings of the Royal Society B: Biological Sciences.

[41]  Michael Wink,et al.  Biochemistry of plant secondary metabolism. , 2010 .

[42]  J. Gershenzon,et al.  Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. , 2009, Phytochemistry.

[43]  Jeffrey A. Riffell,et al.  Characterization and Coding of Behaviorally Significant Odor Mixtures , 2009, Current Biology.

[44]  J. Kingsolver,et al.  PHENOTYPIC SELECTION , 2009 .

[45]  P. Nosil,et al.  Speciation and Patterns of Diversity: Niche dimensionality and ecological speciation , 2009 .

[46]  Steve Horvath,et al.  WGCNA: an R package for weighted correlation network analysis , 2008, BMC Bioinformatics.

[47]  Christian Peter Klingenberg,et al.  Morphological Integration and Developmental Modularity , 2008 .

[48]  M. Elgar,et al.  The evolution of pheromone diversity. , 2008, Trends in ecology & evolution.

[49]  J. Gershenzon,et al.  Diversity and distribution of floral scent , 2006, The Botanical Review.

[50]  J. Arroyo,et al.  Differences in pollinator faunas may generate geographic differences in floral morphology and integration in Narcissus papyraceus (Amaryllidaceae) , 2007 .

[51]  S. Binder,et al.  Branched‐chain amino acid metabolism in higher plants , 2007 .

[52]  K. Matsui.  Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. , 2006, Current opinion in plant biology.

[53]  E. Pichersky,et al.  The Chemical Diversity of Floral Scent , 2006 .

[54]  Eran Pichersky,et al.  Biology of floral scent , 2006 .

[55]  R. Yamaoka,et al.  Ant Nestmate and Non-Nestmate Discrimination by a Chemosensory Sensillum , 2005, Science.

[56]  Christine Woodcock,et al.  Insect host location: a volatile situation. , 2005, Trends in plant science.

[57]  Sarah R Partan,et al.  Issues in the Classification of Multimodal Communication Signals , 2005, The American Naturalist.

[58]  J. Gershenzon,et al.  Two sesquiterpene synthases are responsible for the complex mixture of sesquiterpenes emitted from Arabidopsis flowers. , 2005, The Plant journal : for cell and molecular biology.

[59]  Ted C. J. Turlings,et al.  Recruitment of entomopathogenic nematodes by insect-damaged maize roots , 2005, Nature.

[60]  Kazushige Touhara,et al.  Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[61]  D. Papaj,et al.  Complex signal function: developing a framework of testable hypotheses , 2004, Behavioral Ecology and Sociobiology.

[62]  P. Shannon,et al.  Cytoscape: a software environment for integrated models of biomolecular interaction networks. , 2003, Genome research.

[63]  T. Garland,et al.  TESTING FOR PHYLOGENETIC SIGNAL IN COMPARATIVE DATA: BEHAVIORAL TRAITS ARE MORE LABILE , 2003, Evolution; international journal of organic evolution.

[64]  M. Pigliucci.  Phenotypic integration: studying the ecology and evolution of complex phenotypes , 2003 .

[65]  Ivo Feussner,et al.  The lipoxygenase pathway. , 2003, Annual review of plant biology.

[66]  X. Cerdá,et al.  Floral integration, phenotypic covariance structure and pollinator variation in bumblebee‐pollinated Helleborus foetidus , 2002 .

[67]  Masaomi Teshigawara,et al.  Structural Design Principles , 2001 .

[68]  W. Eisenreich,et al.  Deoxyxylulose phosphate pathway to terpenoids. , 2001, Trends in plant science.

[69]  Barkman.  Character coding of secondary chemical variation for use in phylogenetic analyses. , 2001, Biochemical systematics and ecology.

[70]  B. Hansson,et al.  Sex or Food? Appetetive Learning of Sex Odors in a Male Moth , 1999, Naturwissenschaften.

[71]  G. J. Blomquist,et al.  Insect pheromones--an overview of biosynthesis and endocrine regulation. , 1999, Insect biochemistry and molecular biology.

[72]  M. Kehat,et al.  Sex pheromones: Achievements in monitoring and mating disruption of cotton pests in Israel , 1993 .

[73]  Christer Löfstedt,et al.  Population variation and genetic control of pheromone communication systems in moths , 1990 .

[74]  Günter P. Wagner,et al.  On the eigenvalue distribution of genetic and phenotypic dispersion matrices: Evidence for a nonrandom organization of quantitative character variation , 1984 .

[75]  S. J. Arnold,et al.  THE MEASUREMENT OF SELECTION ON CORRELATED CHARACTERS , 1983, Evolution; international journal of organic evolution.

[76]  R. L. Berg,et al.  THE ECOLOGICAL SIGNIFICANCE OF CORRELATION PLEIADES , 1960 .

[77]  Richard M. Caprioli,et al.  Defensive Function of Herbivore-Induced Plant Volatile Emissions in Nature , 2022 .