Covariation and phenotypic integration in chemical communication displays

biosynthetic constraints and eco-evolutionary implications

Robert R. Junker*, Jonas Kuppler, Luisa Amo, James D. Blande, Renee M. Borges, Nicole M. van Dam, Marcel Dicke, Stefan Dötterl, Bodil K. Ehlers, Florian Etl, Jonathan Gershenzon, Robert Glinwood, Rieta Gols, Astrid T. Groot, Martin Heil, Mathias Hoffmeister, Jarmo K. Holopainen, Stefan Jarau, Lena John, Andre Kessler & 20 others Jette T. Knudsen, Christian Kost, Anne Amélie C. Larue-Kontic, Sara Diana Leonhardt, Dani Lucas-Barbosa, Cassie J. Majetic, Florian Menzel, Amy L. Parachnowitsch, Rémy S. Pasquet, Erik H. Poelman, Robert A. Raguso, Joachim Ruther, Florian P. Schiestl, Thomas Schmitt, Dorothea Tholl, Sybille B. Unsicker, Niels Verhulst, Marcel E. Visser, Berhane T. Weldegergis, Tobias G. Köllner

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

27 Citations (Scopus)

Abstract

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.

Original languageEnglish
Pages (from-to)739-749
JournalNew Phytologist
Volume220
Issue number3
DOIs
Publication statusPublished - Nov 2018

Fingerprint

animal communication
Animal Communication
Herbivory
Pheromones
animals
Acoustics
insect pheromones
Insects
Meta-Analysis
Communication
meta-analysis
pollinators
trajectories
acoustics
antagonists
physicochemical properties
herbivores
odors

Keywords

  • biosynthetic constraints
  • chemical communication
  • correlation network analysis
  • floral scents
  • phenotypic integration
  • vegetative scents

Cite this

Junker, R. R., Kuppler, J., Amo, L., Blande, J. D., Borges, R. M., van Dam, N. M., ... Köllner, T. G. (2018). Covariation and phenotypic integration in chemical communication displays: biosynthetic constraints and eco-evolutionary implications. New Phytologist, 220(3), 739-749. https://doi.org/10.1111/nph.14505
Junker, Robert R. ; Kuppler, Jonas ; Amo, Luisa ; Blande, James D. ; Borges, Renee M. ; van Dam, Nicole M. ; Dicke, Marcel ; Dötterl, Stefan ; Ehlers, Bodil K. ; Etl, Florian ; Gershenzon, Jonathan ; Glinwood, Robert ; Gols, Rieta ; Groot, Astrid T. ; Heil, Martin ; Hoffmeister, Mathias ; Holopainen, Jarmo K. ; Jarau, Stefan ; John, Lena ; Kessler, Andre ; Knudsen, Jette T. ; Kost, Christian ; Larue-Kontic, Anne Amélie C. ; Leonhardt, Sara Diana ; Lucas-Barbosa, Dani ; Majetic, Cassie J. ; Menzel, Florian ; Parachnowitsch, Amy L. ; Pasquet, Rémy S. ; Poelman, Erik H. ; Raguso, Robert A. ; Ruther, Joachim ; Schiestl, Florian P. ; Schmitt, Thomas ; Tholl, Dorothea ; Unsicker, Sybille B. ; Verhulst, Niels ; Visser, Marcel E. ; Weldegergis, Berhane T. ; Köllner, Tobias G. / Covariation and phenotypic integration in chemical communication displays : biosynthetic constraints and eco-evolutionary implications. In: New Phytologist. 2018 ; Vol. 220, No. 3. pp. 739-749.
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abstract = "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.",
keywords = "biosynthetic constraints, chemical communication, correlation network analysis, floral scents, phenotypic integration, vegetative scents",
author = "Junker, {Robert R.} and Jonas Kuppler and Luisa Amo and Blande, {James D.} and Borges, {Renee M.} and {van Dam}, {Nicole M.} and Marcel Dicke and Stefan D{\"o}tterl and Ehlers, {Bodil K.} and Florian Etl and Jonathan Gershenzon and Robert Glinwood and Rieta Gols and Groot, {Astrid T.} and Martin Heil and Mathias Hoffmeister and Holopainen, {Jarmo K.} and Stefan Jarau and Lena John and Andre Kessler and Knudsen, {Jette T.} and Christian Kost and Larue-Kontic, {Anne Am{\'e}lie C.} and Leonhardt, {Sara Diana} and Dani Lucas-Barbosa and Majetic, {Cassie J.} and Florian Menzel and Parachnowitsch, {Amy L.} and Pasquet, {R{\'e}my S.} and Poelman, {Erik H.} and Raguso, {Robert A.} and Joachim Ruther and Schiestl, {Florian P.} and Thomas Schmitt and Dorothea Tholl and Unsicker, {Sybille B.} and Niels Verhulst and Visser, {Marcel E.} and Weldegergis, {Berhane T.} and K{\"o}llner, {Tobias G.}",
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pages = "739--749",
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Junker, RR, Kuppler, J, Amo, L, Blande, JD, Borges, RM, van Dam, NM, Dicke, M, Dötterl, S, Ehlers, BK, Etl, F, Gershenzon, J, Glinwood, R, Gols, R, Groot, AT, Heil, M, Hoffmeister, M, Holopainen, JK, Jarau, S, John, L, Kessler, A, Knudsen, JT, Kost, C, Larue-Kontic, AAC, Leonhardt, SD, Lucas-Barbosa, D, Majetic, CJ, Menzel, F, Parachnowitsch, AL, Pasquet, RS, Poelman, EH, Raguso, RA, Ruther, J, Schiestl, FP, Schmitt, T, Tholl, D, Unsicker, SB, Verhulst, N, Visser, ME, Weldegergis, BT & Köllner, TG 2018, 'Covariation and phenotypic integration in chemical communication displays: biosynthetic constraints and eco-evolutionary implications', New Phytologist, vol. 220, no. 3, pp. 739-749. https://doi.org/10.1111/nph.14505

Covariation and phenotypic integration in chemical communication displays : biosynthetic constraints and eco-evolutionary implications. / Junker, Robert R.; Kuppler, Jonas; Amo, Luisa; Blande, James D.; Borges, Renee M.; van Dam, Nicole M.; Dicke, Marcel; Dötterl, Stefan; Ehlers, Bodil K.; Etl, Florian; Gershenzon, Jonathan; Glinwood, Robert; Gols, Rieta; Groot, Astrid T.; Heil, Martin; Hoffmeister, Mathias; Holopainen, Jarmo K.; Jarau, Stefan; John, Lena; Kessler, Andre; Knudsen, Jette T.; Kost, Christian; Larue-Kontic, Anne Amélie C.; Leonhardt, Sara Diana; Lucas-Barbosa, Dani; Majetic, Cassie J.; Menzel, Florian; Parachnowitsch, Amy L.; Pasquet, Rémy S.; Poelman, Erik H.; Raguso, Robert A.; Ruther, Joachim; Schiestl, Florian P.; Schmitt, Thomas; Tholl, Dorothea; Unsicker, Sybille B.; Verhulst, Niels; Visser, Marcel E.; Weldegergis, Berhane T.; Köllner, Tobias G.

In: New Phytologist, Vol. 220, No. 3, 11.2018, p. 739-749.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Covariation and phenotypic integration in chemical communication displays

T2 - biosynthetic constraints and eco-evolutionary implications

AU - Junker, Robert R.

AU - Kuppler, Jonas

AU - Amo, Luisa

AU - Blande, James D.

AU - Borges, Renee M.

AU - van Dam, Nicole M.

AU - Dicke, Marcel

AU - Dötterl, Stefan

AU - Ehlers, Bodil K.

AU - Etl, Florian

AU - Gershenzon, Jonathan

AU - Glinwood, Robert

AU - Gols, Rieta

AU - Groot, Astrid T.

AU - Heil, Martin

AU - Hoffmeister, Mathias

AU - Holopainen, Jarmo K.

AU - Jarau, Stefan

AU - John, Lena

AU - Kessler, Andre

AU - Knudsen, Jette T.

AU - Kost, Christian

AU - Larue-Kontic, Anne Amélie C.

AU - Leonhardt, Sara Diana

AU - Lucas-Barbosa, Dani

AU - Majetic, Cassie J.

AU - Menzel, Florian

AU - Parachnowitsch, Amy L.

AU - Pasquet, Rémy S.

AU - Poelman, Erik H.

AU - Raguso, Robert A.

AU - Ruther, Joachim

AU - Schiestl, Florian P.

AU - Schmitt, Thomas

AU - Tholl, Dorothea

AU - Unsicker, Sybille B.

AU - Verhulst, Niels

AU - Visser, Marcel E.

AU - Weldegergis, Berhane T.

AU - Köllner, Tobias G.

PY - 2018/11

Y1 - 2018/11

N2 - 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.

AB - 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.

KW - biosynthetic constraints

KW - chemical communication

KW - correlation network analysis

KW - floral scents

KW - phenotypic integration

KW - vegetative scents

U2 - 10.1111/nph.14505

DO - 10.1111/nph.14505

M3 - Article

VL - 220

SP - 739

EP - 749

JO - New Phytologist

JF - New Phytologist

SN - 0028-646X

IS - 3

ER -