Brief sensory experience differentially affects the volume of olfactory brain centres in a moth

Anton, Sylvia; Chabaud, Marie-Ange; Schmidt-Büsser, Daniela; Gadenne, Bruno; Iqbal, Javaid; Juchaux, Marjorie; List, Olivier; Gaertner, Cyril; Devaud, Jean-Marc

doi:10.1007/s00441-015-2299-0

Cited by 18 publications

(26 citation statements)

References 37 publications

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“…Brief exposures to odors were previously shown to impact the expression of olfactory receptors, odorant binding proteins, and the development of brain olfactory centers in honeybees and moths (31–34). In the bee, qRT-PCR analysis revealed that 6 floral scent receptors were differentially expressed in the antenna depending on the scent environment they experienced (31).…”

Section: Discussionmentioning

confidence: 99%

“…In the bee, qRT-PCR analysis revealed that 6 floral scent receptors were differentially expressed in the antenna depending on the scent environment they experienced (31). A brief one-minute exposure of male moths to female sex pheromones led to the up-regulation of a pheromone-binding protein in the male antennae, an enlargement of the antennal lobe, and an increase in the volume of the mushroom bodies in the male brain, which resulted in a higher sensitivity of the exposed males to the female blend (32–34). The brief exposure of B. anynana females to the new male pheromone blend may have led to similar changes in the female brain.…”

Section: Discussionmentioning

confidence: 99%

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Early-exposure to new sex pheromone blend alters mate preference in female butterflies and in their offspring

Dion

Pui

Monteiro

2017

Preprint

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Insects use species-specific sex pheromone blends to attract members of the opposite sex which express the corresponding molecular receptors. Given this lock and key mechanism used for species identification and mate choice, it is currently not well understood how pheromone blends or receptor systems evolve. One possibility is that insects develop preferences for new sex pheromone blends via the process of learning, and that these learned preferences may be passed on to the next generation. We tested these hypotheses by exposing newly emerged Bicyclus anynana female butterflies to either wild type or to modified male sex pheromone blends. A few days later, we scored female mating outcome in a choice trial involving both male types. We also assessed the mating outcome of naïve offspring of females that underwent distinct odor learning trials to test for a potential inheritance of learned odor preferences. Naïve (parental) females mated preferentially with Wt-blend males, but females pre-exposed to new blends either shifted their preference to new-blend males, or mated equally with males of either blend type; the response depending on the new blend they were introduced to. Naïve daughters of females who were exposed to new-blend males behaved similarly to their experienced mothers. We demonstrate that females are able to learn preferences for novel pheromone blends in response to a short social experience, and pass that learned preference down to the next generation. This suggests that learning can be a key factor in the evolution of sex pheromone blend recognition and in chemosensory speciation.Significance statementWhile the diversity of sex pheromone communication systems across insects is well documented, the mechanisms that lead to such diversity are not well understood. Sex pheromones constitute a species-specific system of sexual communication that reinforces interspecific reproductive isolation. When odor blends evolve, the efficacy of male-female communication becomes compromised, unless preference for novel blends also evolves. We explore odor learning as a possible mechanism leading to changes in sex pheromone preferences. We show that preferences for new blends can develop following a short learning experience, and that these novel preferences can be transmitted to the next generation. To our knowledge, this is the first investigation of sex pheromone blend preference learning impacting mate choice and being inherited in an insect.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Early-exposure to new sex pheromone blend alters mate preference in female butterflies and in their offspring

Dion

Pui

Monteiro

2017

Preprint

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“…In insects, various behaviors are modulated in response to physiological or environmental changes, such as experience, mating, age or time of the day (review in Martel et al, 2009). In most species, this behavioral plasticity is mainly sustained by a modulation of the central olfactory system (antennal lobes and mushroom bodies, see e.g., Barrozo et al, 2011;Anton et al, 2015). But as antennae are the first place of odorant detection, modulation can also take place at this peripheral level.…”

Section: Discussionmentioning

confidence: 99%

Expression and modulation of neuroligin and neurexin in the olfactory organ of the cotton leaf worm Spodoptera littoralis

et al. 2016

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Carboxylesterases are enzymes widely distributed within living organisms. In insects, they have been mainly involved in dietary metabolism and detoxification function. Interestingly, several members of this family called carboxylesterase-like adhesion molecules (CLAMs) have lost their catalytic properties and are mainly involved in neuro/developmental functions. CLAMs include gliotactins, neurotactins, glutactins, and neuroligins. The latter have for binding partner the neurexin. In insects, the function of these proteins has been mainly studied in Drosophila central nervous system or neuromuscular junction. Some studies suggested a role of neuroligins and neurexin in sensory processing but CLAM expression within sensory systems has not been investigated. Here, we reported the identification of 5 putative CLAMs expressed in the olfactory system of the model pest insect Spodoptera littoralis. One neuroligin, Slnlg4-yll and its putative binding partner neurexin SlnrxI were the most expressed in the antennae and were surprisingly associated with olfactory sensilla. In addition, both transcripts were upregulated in male antennae after mating, known to modulate the sensitivity of the peripheral olfactory system in S. littoralis, suggesting that these molecules could be involved in sensory plasticity.

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“…littoralis is modified by brief pre-exposure, eliciting increased sensitivity of peripheral and more pronouncedly in AL neurons as well as an increase in the volume of the pheromone-processing cumulus of the macroglomerular complex within the antennal lobe and the calyces of the secondary olfactory centres, the mushroom bodies [25, 27, 28], nothing is known so far on the neuromodulators potentially involved in these changes.…”

Section: Discussionmentioning

confidence: 99%

“…Such a type of olfactory plasticity based on non-associative learning has been unveiled in the moth Spodoptera littoralis : a brief pre-exposure to sex pheromone enhances behavioural responses to sex pheromone 15 min and 24 h later [25, 26]. Pheromone exposure was also shown to enhance peripheral pheromone detection, central nervous pheromone responses, and to induce an increase in the volume of certain glomeruli and specifically the size of the biggest glomerulus processing the main pheromone component within the antennal lobe (AL), the primary olfactory centre, as well as in a secondary olfactory centre, the calyces of the mushroom bodies [25, 27, 28]. It is so far unknown if such pre-exposure effects are also present in other insects and if they depend on the physiological state of the insect.…”

Section: Introductionmentioning

confidence: 99%

An Insecticide Further Enhances Experience-Dependent Increased Behavioural Responses to Sex Pheromone in a Pest Insect

et al. 2016

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Neonicotinoid insecticides are widely used to protect plants against pest insects, and insecticide residues remaining in the environment affect both target and non-target organisms. Whereas low doses of neonicotinoids have been shown to disturb the behaviour of pollinating insects, recent studies have revealed that a low dose of the neonicotinoid clothianidin can improve behavioural and neuronal sex pheromone responses in a pest insect, the male moth Agrotis ipsilon, and thus potentially improve reproduction. As male moth behaviour depends also on its physiological state and previous experience with sensory signals, we wondered if insecticide effects would be dependent on plasticity of olfactory-guided behaviour. We investigated, using wind tunnel experiments, whether a brief pre-exposure to the sex pheromone could enhance the behavioural response to this important signal in the moth A. ipsilon at different ages (sexually immature and mature males) and after different delays (2 h and 24 h), and if the insecticide clothianidin would interfere with age effects or the potential pre-exposure-effects. Brief pre-exposure to the pheromone induced an age-independent significant increase of sex pheromone responses 24 h later, whereas sex pheromone responses did not increase significantly 2 h after exposure. However, response delays were significantly shorter compared to naïve males already two hours after exposure. Oral treatment with clothianidin increased sex pheromone responses in sexually mature males, confirming previous results, but did not influence responses in young immature males. Males treated with clothianidin after pre-exposure at day 4 responded significantly more to the sex pheromone at day 5 than males treated with clothianidin only and than males pre-exposed only, revealing an additive effect of experience and the insecticide. Plasticity of sensory systems has thus to be taken into account when investigating the effects of sublethal doses of insecticides on behaviour.

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Brief sensory experience differentially affects the volume of olfactory brain centres in a moth

Cited by 18 publications

References 37 publications

Early-exposure to new sex pheromone blend alters mate preference in female butterflies and in their offspring

Early-exposure to new sex pheromone blend alters mate preference in female butterflies and in their offspring

Expression and modulation of neuroligin and neurexin in the olfactory organ of the cotton leaf worm Spodoptera littoralis

An Insecticide Further Enhances Experience-Dependent Increased Behavioural Responses to Sex Pheromone in a Pest Insect

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