Unique neural coding of crucial versus irrelevant plant odors in a hawkmoth
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Evaluation Summary:
This manuscript is of particular interest to researchers in the fields of neuroecology of insect olfaction and of insect-plant interactions in general. The authors investigate the olfactory signals that guide the specialist hawkmoth Manduca sexta towards plants that are used for oviposition and for nectar-feeding in a natural setting. How insects distinguish useful information from irrelevant information is an important question. The authors use elegant chemical ecology techniques and recordings of neuronal activity to ask how female moths (Manduca sexta) could discriminate co-occurring behaviorally relevant vs irrelevant plant and floral volatiles.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #3 agreed to share their name with the authors.)
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Abstract
The sense of smell is pivotal for nocturnal moths to locate feeding and oviposition sites. However, these crucial resources are often rare and their bouquets are intermingled with volatiles emanating from surrounding ‘background’ plants. Here, we asked if the olfactory system of female hawkmoths, Manduca sexta , could differentiate between crucial and background cues. To answer this question, we collected nocturnal headspaces of numerous plants in a natural habitat of M. sexta . We analyzed the chemical composition of these headspaces and used them as stimuli in physiological experiments at the antenna and in the brain. The intense odors of floral nectar sources evoked strong responses in virgin and mated female moths, most likely enabling the localization of profitable flowers at a distance. Bouquets of larval host plants and most background plants, in contrast, were subtle, thus potentially complicating host identification. However, despite being subtle, antennal responses and brain activation patterns evoked by the smell of larval host plants were clearly different from those evoked by other plants. Interestingly, this difference was even more pronounced in the antennal lobe of mated females, revealing a status-dependent tuning of their olfactory system towards oviposition sites. Our study suggests that female moths possess unique neural coding strategies to find not only conspicuous floral cues but also inconspicuous bouquets of larval host plants within a complex olfactory landscape.
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Author Response
Reviewer #2 (Public Review):
Studying the olfactory encoding strategies of moths using ecologically relevant odors collected from the actual habitat is remarkably ambitious. The manuscript is well written and the design of the experiment is clear.
We thank the reviewer for this positive evaluation of our study.
The authors collected the nocturnal emission of 16 plant species and systematically analyzed the constitution of the headspace of these plants. Then, they used GC-EAD to identify the active compounds and found 77 EAD-active ones in total. Subsequently, they used in vivo calcium imaging to study the representation of these active compounds in antennal lobes. A weakness is the absence of behavioral data.
The plants that are of ecological relevance for M. sexta as nectar sources and oviposition sites are known …
Author Response
Reviewer #2 (Public Review):
Studying the olfactory encoding strategies of moths using ecologically relevant odors collected from the actual habitat is remarkably ambitious. The manuscript is well written and the design of the experiment is clear.
We thank the reviewer for this positive evaluation of our study.
The authors collected the nocturnal emission of 16 plant species and systematically analyzed the constitution of the headspace of these plants. Then, they used GC-EAD to identify the active compounds and found 77 EAD-active ones in total. Subsequently, they used in vivo calcium imaging to study the representation of these active compounds in antennal lobes. A weakness is the absence of behavioral data.
The plants that are of ecological relevance for M. sexta as nectar sources and oviposition sites are known and well documented both from observations in the field and behavioral experiments in the lab (see references in the introduction of our manuscript). We use headspace of these plants with known ecological meaning and of many other plants present in the direct neighborhood to test how female hawkmoths perceive relevant and irrelevant plant bouquets at the antenna and how these headspaces are spatially coded in the antennal lobe. It is, therefore, difficult to understand in which respect the unspecified ‘behavioral data’ the reviewer asked for might add further information to our study.
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Evaluation Summary:
This manuscript is of particular interest to researchers in the fields of neuroecology of insect olfaction and of insect-plant interactions in general. The authors investigate the olfactory signals that guide the specialist hawkmoth Manduca sexta towards plants that are used for oviposition and for nectar-feeding in a natural setting. How insects distinguish useful information from irrelevant information is an important question. The authors use elegant chemical ecology techniques and recordings of neuronal activity to ask how female moths (Manduca sexta) could discriminate co-occurring behaviorally relevant vs irrelevant plant and floral volatiles.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the …
Evaluation Summary:
This manuscript is of particular interest to researchers in the fields of neuroecology of insect olfaction and of insect-plant interactions in general. The authors investigate the olfactory signals that guide the specialist hawkmoth Manduca sexta towards plants that are used for oviposition and for nectar-feeding in a natural setting. How insects distinguish useful information from irrelevant information is an important question. The authors use elegant chemical ecology techniques and recordings of neuronal activity to ask how female moths (Manduca sexta) could discriminate co-occurring behaviorally relevant vs irrelevant plant and floral volatiles.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #3 agreed to share their name with the authors.)
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Reviewer #1 (Public Review):
Bisch-Knaden et al. investigated how the olfactory system of hawkmoths (Manduca sexta) could distinguish behaviorally relevant odor sources (nectar food sources and oviposition sites) from those which are irrelevant in a natural environment. This is of particular interest for the field of naturalistic insect-plant interactions. Technically and intellectually, the experiments are well-conducted and suited to understand how ecologically relevant naturally-occurring signals are processed in the brain of animals to produce adaptive behavior.
The authors collect volatiles from various (behaviorally relevant and irrelevant) plant sources in Southern Arizona (US), a natural habitat of M. sexta. They describe in detail the chemical composition and bioactivity of two floral sources which are important nectar …
Reviewer #1 (Public Review):
Bisch-Knaden et al. investigated how the olfactory system of hawkmoths (Manduca sexta) could distinguish behaviorally relevant odor sources (nectar food sources and oviposition sites) from those which are irrelevant in a natural environment. This is of particular interest for the field of naturalistic insect-plant interactions. Technically and intellectually, the experiments are well-conducted and suited to understand how ecologically relevant naturally-occurring signals are processed in the brain of animals to produce adaptive behavior.
The authors collect volatiles from various (behaviorally relevant and irrelevant) plant sources in Southern Arizona (US), a natural habitat of M. sexta. They describe in detail the chemical composition and bioactivity of two floral sources which are important nectar resources for the moth, the jimsonweed Datura wrightii (which is also used by the moths for oviposition), and the agave species Agave palmieri, which is used only for feeding. Much of this has been described in a series of papers published between 2008-2014 (few of which are cited and/or discussed), which described the chemical composition and bioactivity of components in the floral odor of D. wrightii and A. palmieri, and how those two nectar sources differentially activate neurons in the primary olfactory centers of the brain. How the brain of moths could identify a behaviorally relevant odor bouquet (such as the floral scent of D. wrightii) in an environment of irrelevant odors (e.g. creosote bush) has also been previously examined.
The authors do an impressive work imaging activity in the primary olfactory centers, the ALs, in a model system for which neuronal markers that could facilitate this are not available, and understandable, they can only image accessible/identifiable glomeruli (ca. one third of all glomeruli). Hence, their conclusions necessarily apply only to those glomeruli imaged, and hence it cannot be concluded that vegetative host-plant volatiles are weak activators, because two-thirds of the glomeruli could not be imaged. Various previous reports used electrophysiological recordings in this brain region, which may be more sensitive to detect bioactivity, including inhibitory responses and correlations in the temporal domain. Also, previous work highly suggests that females rely on D. wrightii floral odors to find oviposition sites and therefore, the reported finding that vegetative odors are not strong activators may not be relevant in this case. Electrophysiological recordings from antennal lobe female-specific neurons with selectivity for certain D. wrightii floral odors further support this idea.
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Reviewer #2 (Public Review):
Studying the olfactory encoding strategies of moths using ecologically relevant odors collected from the actual habitat is remarkably ambitious. The manuscript is well written and the design of the experiment is clear.
The authors collected the nocturnal emission of 16 plant species and systematically analyzed the constitution of the headspace of these plants. Then, they used GC-EAD to identify the active compounds and found 77 EAD-active ones in total. Subsequently, they used in vivo calcium imaging to study the representation of these active compounds in antennal lobes. A weakness is the absence of behavioral data.
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Reviewer #3 (Public Review):
The authors' used state of the art approaches to analyse the volatiles emitted by plants in the natural environment of the hawkmoth Manduca sexta, which play different roles in their biology. They then investigated antennal detection of the identified compounds, as well as the representation of odour bouquets of flowering plants (used for feeding), larval host plants (used for oviposition), and surrounding non-host plants. They analysed their data with sophisticated methods and illustrate their results with highly comprehensive figures, which make the results easy to catch for the reader. The results show that flowering plants used for nectar feeding emit large amounts of volatiles and the identified compounds are equally well detected by the antennae and similarly represented within the antennal lobe in …
Reviewer #3 (Public Review):
The authors' used state of the art approaches to analyse the volatiles emitted by plants in the natural environment of the hawkmoth Manduca sexta, which play different roles in their biology. They then investigated antennal detection of the identified compounds, as well as the representation of odour bouquets of flowering plants (used for feeding), larval host plants (used for oviposition), and surrounding non-host plants. They analysed their data with sophisticated methods and illustrate their results with highly comprehensive figures, which make the results easy to catch for the reader. The results show that flowering plants used for nectar feeding emit large amounts of volatiles and the identified compounds are equally well detected by the antennae and similarly represented within the antennal lobe in virgin and mated females. Larval host plants emit surprisingly small amounts of volatiles, but M. sexta antennae are still detecting characteristic compounds and more importantly, odour bouquets of these plants elicit specific activation patterns in the antennal lobe in very few glomeruli and this representation changes after mating. Interestingly, odour bouquets of host plants of sympatric hawkmoth species are highly represented within the antennal lobe and this representation takes even more weight in mated females. Lastly the representation of odour bouquets of non-host (background) plants, rather elaborated in virgin females, decreases after mating. All data are very well presented and illustrated. In the discussion, the results are very well put into the context of earlier studies, putting together knowledge on the ecology of hawkmoths, behavioural studies, as well as detection and central processing of plant volatiles and its plasticity. The conclusions drawn, insisting on the ecological adaptation of the female moth olfactory system in order to recognize and discriminate crucial information for feeding and host plant localization as a function of the physiological state, are sound and contribute an important piece of information to our knowledge on neural mechanisms underlying insect behaviour in a highly complex natural environment.
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