Plant-ants use resistance-related plant odours to assess host quality before colony founding

1. Establishing a horizontally transmitted mutualism is a critical step for many organisms, particularly when an individual can engage with only one partner over its lifetime. Ant foundresses shed their wings before they start to lay eggs, which makes host choice particularly critical for plant-ants...

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Published inThe Journal of ecology Vol. 106; no. 1; pp. 379 - 390
Main Authors Razo-Belman, Rosario, Molina-Torres, Jorge, Martínez, Octavio, Heil, Martin
Format Journal Article
LanguageEnglish
Published Oxford John Wiley & Sons Ltd 01.01.2018
Blackwell Publishing Ltd
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ISSN0022-0477
1365-2745
DOI10.1111/1365-2745.12832

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Abstract 1. Establishing a horizontally transmitted mutualism is a critical step for many organisms, particularly when an individual can engage with only one partner over its lifetime. Ant foundresses shed their wings before they start to lay eggs, which makes host choice particularly critical for plant-ants that exclusively colonize myrmecophytes. 2. Volatile organic compounds (VOCs) can indicate the identity and physiological condition of an individual and frequently serve as signals or cues that facilitate partner choice. Thus, we hypothesized that obligate plant-ants use VOCs to determine the quality of potential host plants. 3. Indeed, winged females of the plant-ant, Pseudomyrmex ferrugineus, used plant odours to identify high-quality acacia hosts among different species and among individuals of the same species. The VOC blend of a branch was related to reward production and, interestingly, the least attractive blend contained the highest number of compounds. 4. Although only seven different VOCs could be detected in the blend of the high-reward host species, the low-reward host emitted 13 different compounds, among which (S)-(-)-limonene and β-linalool were the dominant ones. Complementing the odour of the high-reward host with (S)-(-)-limonene, β-linalool or α-terpinene reduced its attractiveness. Strikingly, these compounds inhibited bacterial pathogens of the host plant. 5. Synthesis. Plant-ants can use host plant odours that contain resistance-related VOCs to judge on host quality, likely because of negative crosstalk between direct resistance to disease and investment in ant-mediated defence. VOCs can serve as cues that provide reliable information for partner choice, particularly when their emission results from a physiological process that causally relates to the quality of an individual as a mutualist.
AbstractList 1. Establishing a horizontally transmitted mutualism is a critical step for many organisms, particularly when an individual can engage with only one partner over its lifetime. Ant foundresses shed their wings before they start to lay eggs, which makes host choice particularly critical for plant-ants that exclusively colonize myrmecophytes. 2. Volatile organic compounds (VOCs) can indicate the identity and physiological condition of an individual and frequently serve as signals or cues that facilitate partner choice. Thus, we hypothesized that obligate plant-ants use VOCs to determine the quality of potential host plants. 3. Indeed, winged females of the plant-ant, Pseudomyrmex ferrugineus, used plant odours to identify high-quality acacia hosts among different species and among individuals of the same species. The VOC blend of a branch was related to reward production and, interestingly, the least attractive blend contained the highest number of compounds. 4. Although only seven different VOCs could be detected in the blend of the high-reward host species, the low-reward host emitted 13 different compounds, among which (S)-(-)-limonene and β-linalool were the dominant ones. Complementing the odour of the high-reward host with (S)-(-)-limonene, β-linalool or α-terpinene reduced its attractiveness. Strikingly, these compounds inhibited bacterial pathogens of the host plant. 5. Synthesis. Plant-ants can use host plant odours that contain resistance-related VOCs to judge on host quality, likely because of negative crosstalk between direct resistance to disease and investment in ant-mediated defence. VOCs can serve as cues that provide reliable information for partner choice, particularly when their emission results from a physiological process that causally relates to the quality of an individual as a mutualist.
Establishing a horizontally transmitted mutualism is a critical step for many organisms, particularly when an individual can engage with only one partner over its lifetime. Ant foundresses shed their wings before they start to lay eggs, which makes host choice particularly critical for plant‐ants that exclusively colonize myrmecophytes. Volatile organic compounds (VOCs) can indicate the identity and physiological condition of an individual and frequently serve as signals or cues that facilitate partner choice. Thus, we hypothesized that obligate plant‐ants use VOCs to determine the quality of potential host plants. Indeed, winged females of the plant‐ant, Pseudomyrmex ferrugineus , used plant odours to identify high‐quality acacia hosts among different species and among individuals of the same species. The VOC blend of a branch was related to reward production and, interestingly, the least attractive blend contained the highest number of compounds. Although only seven different VOCs could be detected in the blend of the high‐reward host species, the low‐reward host emitted 13 different compounds, among which (S)‐(‐)‐limonene and β‐linalool were the dominant ones. Complementing the odour of the high‐reward host with (S)‐(‐)‐limonene, β‐linalool or α‐terpinene reduced its attractiveness. Strikingly, these compounds inhibited bacterial pathogens of the host plant. Synthesis . Plant‐ants can use host plant odours that contain resistance‐related VOCs to judge on host quality, likely because of negative crosstalk between direct resistance to disease and investment in ant‐mediated defence. VOCs can serve as cues that provide reliable information for partner choice, particularly when their emission results from a physiological process that causally relates to the quality of an individual as a mutualist.
Establishing a horizontally transmitted mutualism is a critical step for many organisms, particularly when an individual can engage with only one partner over its lifetime. Ant foundresses shed their wings before they start to lay eggs, which makes host choice particularly critical for plant‐ants that exclusively colonize myrmecophytes. Volatile organic compounds (VOCs) can indicate the identity and physiological condition of an individual and frequently serve as signals or cues that facilitate partner choice. Thus, we hypothesized that obligate plant‐ants use VOCs to determine the quality of potential host plants. Indeed, winged females of the plant‐ant, Pseudomyrmex ferrugineus, used plant odours to identify high‐quality acacia hosts among different species and among individuals of the same species. The VOC blend of a branch was related to reward production and, interestingly, the least attractive blend contained the highest number of compounds. Although only seven different VOCs could be detected in the blend of the high‐reward host species, the low‐reward host emitted 13 different compounds, among which (S)‐(‐)‐limonene and β‐linalool were the dominant ones. Complementing the odour of the high‐reward host with (S)‐(‐)‐limonene, β‐linalool or α‐terpinene reduced its attractiveness. Strikingly, these compounds inhibited bacterial pathogens of the host plant. Synthesis. Plant‐ants can use host plant odours that contain resistance‐related VOCs to judge on host quality, likely because of negative crosstalk between direct resistance to disease and investment in ant‐mediated defence. VOCs can serve as cues that provide reliable information for partner choice, particularly when their emission results from a physiological process that causally relates to the quality of an individual as a mutualist.
Establishing a horizontally transmitted mutualism is a critical step for many organisms, particularly when an individual can engage with only one partner over its lifetime. Ant foundresses shed their wings before they start to lay eggs, which makes host choice particularly critical for plant‐ants that exclusively colonize myrmecophytes. Volatile organic compounds (VOCs) can indicate the identity and physiological condition of an individual and frequently serve as signals or cues that facilitate partner choice. Thus, we hypothesized that obligate plant‐ants use VOCs to determine the quality of potential host plants. Indeed, winged females of the plant‐ant, Pseudomyrmex ferrugineus, used plant odours to identify high‐quality acacia hosts among different species and among individuals of the same species. The VOC blend of a branch was related to reward production and, interestingly, the least attractive blend contained the highest number of compounds. Although only seven different VOCs could be detected in the blend of the high‐reward host species, the low‐reward host emitted 13 different compounds, among which (S)‐(‐)‐limonene and β‐linalool were the dominant ones. Complementing the odour of the high‐reward host with (S)‐(‐)‐limonene, β‐linalool or α‐terpinene reduced its attractiveness. Strikingly, these compounds inhibited bacterial pathogens of the host plant. Synthesis. Plant‐ants can use host plant odours that contain resistance‐related VOCs to judge on host quality, likely because of negative crosstalk between direct resistance to disease and investment in ant‐mediated defence. VOCs can serve as cues that provide reliable information for partner choice, particularly when their emission results from a physiological process that causally relates to the quality of an individual as a mutualist. Pseudomyrmex plant‐ant queens use resistance‐related VOCs with direct antibacterial activity to judge on the quality of a future ‘swollen‐thorn Acacia' host. Plant investment in ant‐mediated defence is subject to a trade‐off with direct resistance to disease. Therefore, a low‐quality host cannot suppress the emission of resistance‐related VOCs, which indicate little investment in ant rewards. Figure Modified from Orona‐Tamayo & Heil (2013), and original figure by Alejandro de León.
Establishing a horizontally transmitted mutualism is a critical step for many organisms, particularly when an individual can engage with only one partner over its lifetime. Ant foundresses shed their wings before they start to lay eggs, which makes host choice particularly critical for plant-ants that exclusively colonize myrmecophytes. Volatile organic compounds (VOCs) can indicate the identity and physiological condition of an individual and frequently serve as signals or cues that facilitate partner choice. Thus, we hypothesized that obligate plant-ants use VOCs to determine the quality of potential host plants. Indeed, winged females of the plant-ant, Pseudomyrmex ferrugineus, used plant odours to identify high-quality acacia hosts among different species and among individuals of the same species. The VOC blend of a branch was related to reward production and, interestingly, the least attractive blend contained the highest number of compounds. Although only seven different VOCs could be detected in the blend of the high-reward host species, the low-reward host emitted 13 different compounds, among which (S)-(-)-limonene and [beta]-linalool were the dominant ones. Complementing the odour of the high-reward host with (S)-(-)-limonene, [beta]-linalool or [alpha]-terpinene reduced its attractiveness. Strikingly, these compounds inhibited bacterial pathogens of the host plant. Synthesis. Plant-ants can use host plant odours that contain resistance-related VOCs to judge on host quality, likely because of negative crosstalk between direct resistance to disease and investment in ant-mediated defence. VOCs can serve as cues that provide reliable information for partner choice, particularly when their emission results from a physiological process that causally relates to the quality of an individual as a mutualist.
Author Martínez, Octavio
Razo-Belman, Rosario
Heil, Martin
Molina-Torres, Jorge
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Snippet 1. Establishing a horizontally transmitted mutualism is a critical step for many organisms, particularly when an individual can engage with only one partner...
Establishing a horizontally transmitted mutualism is a critical step for many organisms, particularly when an individual can engage with only one partner over...
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SubjectTerms Acacia
Ants
ant–plant interaction
Bacteria
Body condition
Crosstalk
Cues
Disease resistance
Eggs
females
host choice
Host plants
host preferences
host quality
Hosts
interspecific communication
Limonene
Linalool
Mutualism
Myrmecophily
myrmecophyte
Odor
Odors
Odour
Organic compounds
pathogen resistance
pathogens
Physiology
Plant-herbivore interactions
Pseudomyrmex ferrugineus
Quality
Quality assessment
Reinforcement
signal
Species
swollen‐thorn acacia
Symbiosis
Terpinene
VOCs
Volatile organic compounds
Wings
Title Plant-ants use resistance-related plant odours to assess host quality before colony founding
URI https://www.jstor.org/stable/45029428
https://onlinelibrary.wiley.com/doi/abs/10.1111%2F1365-2745.12832
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https://www.proquest.com/docview/2020901875
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