Differentiation in putative male sex pheromone components across and within populations of the African butterfly <i>Bicyclus anynana</i> as a potential driver of reproductive isolation

Bacquet, Paul; Jong, Maaike de; Brattström, Oskar; Wang, Hong Lei; Molleman, Freerk; Heuskin, Stéphanie; Lognay, George; Löfstedt, Christer; Brakefield, Paul M.; Vanderpoorten, Alain; Nieberding, Caroline M.

doi:10.1002/ece3.2298

Cited by 10 publications

(13 citation statements)

References 99 publications

(174 reference statements)

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“…While traditionally predicted to be under stabilizing selection, intraspecific variation between populations in chemical profiles has been documented in other Lepidoptera (Carde & Allison, 2016). Chemical divergence in putative male sex pheromones between populations of Bicyclus anynana is reported to be as large as differences between Bicyclus species and is greater than predicted by genetic divergence (Bacquet et al, 2016). This is in contrast to what we find here, where interspecific differences are much greater than intraspecific ones.…”

Section: Discussionmentioning

confidence: 99%

Species specificity and intraspecific variation in the chemical profiles of Heliconius butterflies across a large geographic range

Darragh

Montejo‐Kovacevich

Kozak

et al. 2020

Ecology and Evolution

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In many animals, mate choice is important for the maintenance of reproductive isolation between species. Traits important for mate choice and behavioral isolation are predicted to be under strong stabilizing selection within species; however, such traits can also exhibit variation at the population level driven by neutral and adaptive evolutionary processes. Here, we describe patterns of divergence among androconial and genital chemical profiles at inter-and intraspecific levels in mimetic Heliconius butterflies. Most variation in chemical bouquets was found between species, but there were also quantitative differences at the population level. We found a strong correlation between interspecific chemical and genetic divergence, but this correlation varied in intraspecific comparisons. We identified "indicator" compounds characteristic of particular species that included compounds already known to elicit a behavioral response, suggesting an approach for identification of candidate compounds for future behavioral studies in novel systems. Overall, the strong signal of species identity suggests a role for these compounds in species recognition, but with additional potentially neutral variation at the population level. K E Y W O R D Schemical ecology, Lepidoptera, mate choice, pheromones, reproductive isolation, signaling

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Section: Discussionmentioning

confidence: 99%

Species specificity and intraspecific variation in the chemical profiles of Heliconius butterflies across a large geographic range

Darragh

Montejo‐Kovacevich

Kozak

et al. 2020

Ecology and Evolution

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“…However, the learning process that we describe here, by allowing males with divergent blends to reproduce, may mitigate the strength of stabilizing selection, and create opportunities for pheromone blends and reception systems to evolve. A recent study suggested that quantitative and qualitative variations observed in blends within and between natural B. anynana populations are potentially catalyzing ongoing speciation (6). The odor learning ability of B. anynana females has probably maintained the high variance in MSP amounts measured in different stock populations (24, 25, 30), as 225 well as the variance in MSPs detected across natural populations (6).…”

Section: Discussionmentioning

confidence: 99%

“…A recent study suggested that quantitative and qualitative variations observed in blends within and between natural B. anynana populations are potentially catalyzing ongoing speciation (6). The odor learning ability of B. anynana females has probably maintained the high variance in MSP amounts measured in different stock populations (24, 25, 30), as 225 well as the variance in MSPs detected across natural populations (6). Furthermore, the use of multimodal signals in mate selection in B. anynana , where females use both olfactory and visual signals to assess mate quality (11, 23, 28), may facilitate pheromone learning and the evolution of the MSP blends.…”

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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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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“…However, the learning process that we describe here, by allowing males with divergent blends to reproduce, may mitigate the strength of stabilizing selection, and create opportunities for pheromone blends and reception systems to evolve. A recent study suggested that quantitative and qualitative variations observed in blends within and between natural B. anynana populations are potentially catalyzing ongoing speciation 6 . The odor learning ability of B. anynana females has probably maintained the high variance in MSP amounts measured in different stock populations 28,30,33 , as well as the variance in MSPs detected across natural populations 6 .…”

Section: Discussionmentioning

confidence: 99%

“…A recent study suggested that quantitative and qualitative variations observed in blends within and between natural B. anynana populations are potentially catalyzing ongoing speciation 6 . The odor learning ability of B. anynana females has probably maintained the high variance in MSP amounts measured in different stock populations 28,30,33 , as well as the variance in MSPs detected across natural populations 6 . Furthermore, the use of multimodal signals in mate selection in B. anynana , where females use both olfactory and visual cues to assess mate quality 12,26,27 , may facilitate pheromone learning and the evolution of the MSP blends.…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2020

View full text Add to dashboard Cite

While 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 in the butterfly Bicyclus anynana. Our experiments reveal mating patterns suggesting that mating bias for new blends can develop following a short learning experience, and that this maternal experience impacts the mating outcome of offspring without further exposure. We propose that odor learning can be a key factor in the evolution of sex pheromone blend recognition and in chemosensory speciation.

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Differentiation in putative male sex pheromone components across and within populations of the African butterfly Bicyclus anynana as a potential driver of reproductive isolation

Cited by 10 publications

References 99 publications

Species specificity and intraspecific variation in the chemical profiles of Heliconius butterflies across a large geographic range

Species specificity and intraspecific variation in the chemical profiles of Heliconius butterflies across a large geographic range

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

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

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