Sensory specificity and speciation: a potential neuronal pathway for host fruit odour discrimination in
            <i>Rhagoletis pomonella</i>

Tait, Cheyenne; Batra, Srishti; Ramaswamy, Sree Subha; Feder, Jeffrey L.; Olsson, Shannon B.

doi:10.1098/rspb.2016.2101

Cited by 31 publications

(32 citation statements)

References 53 publications

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“…Similar divergence in peripheral nervous system architecture has been seen in Rhagoletis pomonella (Frey and Bush ; Tait et al. ) and Drosophila mojavensis (Date et al. ; Crowley‐Gall et al.…”

Section: Discussionsupporting

confidence: 61%

A major locus controls a biologically active pheromone component inHeliconius melpomene

et al. 2020

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Understanding the production, response, and genetics of signals used in mate choice can inform our understanding of the evolution of both intraspecific mate choice and reproductive isolation. Sex pheromones are important for courtship and mate choice in many insects, but we know relatively little of their role in butterflies. The butterfly Heliconius melpomene uses a complex blend of wing androconial compounds during courtship. Electroantennography in H. melpomene and its close relative Heliconius cydno showed that responses to androconial extracts were not species specific. Females of both species responded equally strongly to extracts of both species, suggesting conservation of peripheral nervous system elements across the two species. Individual blend components provoked little to no response, with the exception of octadecanal, a major component of the H. melpomene blend. Supplementing octadecanal on the wings of octadecanal‐rich H. melpomene males led to an increase in the time until mating, demonstrating the bioactivity of octadecanal in Heliconius. Using quantitative trait locus (QTL) mapping, we identified a single locus on chromosome 20 responsible for 41% of the parental species’ difference in octadecanal production. This QTL does not overlap with any of the major wing color or mate choice loci, nor does it overlap with known regions of elevated or reduced FST. A set of 16 candidate fatty acid biosynthesis genes lies underneath the QTL. Pheromones in Heliconius carry information relevant for mate choice and are under simple genetic control, suggesting they could be important during speciation.

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Section: Discussionsupporting

confidence: 61%

A major locus controls a biologically active pheromone component inHeliconius melpomene

et al. 2020

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“…For example, the moth Ostrinia nubialis , whose E -and Z-strains diverged approximately 75,000-150,000 years ago (Malausa et al 2007), strains have opposite topologies in the antennal lobe and antennal sensillae (Kárpáti et al 2007; Koutroumpa et al 2014). Similar divergence in peripheral nervous system architecture has been seen in Rhagoletis pomonella (Frey and Bush 1990; Tait et al 2016) and Drosophila mojavensis (Date et al 2013; Crowley-Gall et al 2016) despite much shorter divergence times than between H. melpomene and H. cydno (approximately 2.1 million years ago, Arias et al 2014; Kozak et al 2015).…”

Section: Discussionmentioning

confidence: 52%

“…These data stand in marked contrast to similar studies in other insect species and suggest that the peripheral nervous system architecture of H. melpomene and H. cydno has not diverged alongside their wing pheromone components. By contrast, the moth Ostrinia nubialis , whose E - and Z -strains diverged approximately 75,000-150,000 years ago (Malausa et al 2007), have opposite topologies in the antennal lobe and antennal sensillae (Kárpáti et al 2008, Koutroumpa et al 2014), and similar divergence in peripheral nervous system architecture has been seen in Rhagoletis pomonella (Frey & Bush 1990, Tait et al 2016) and Drosophila mojavensis (Date et al 2013, Crowley-Gall et al 2016) despite much shorter divergence times than between H. melpomene and H. cydno . Our results in Heliconius parallel what is seen in Colias butterflies, where C. eurytheme and C. philodice show very similar female electrophysiological responses to the con- and heterospecific pheromone compounds, despite a behavioral effect of treating males with heterospecific pheromones (Grula et al 1980).…”

Section: Discussionmentioning

confidence: 99%

A major locus controls a biologically active pheromone component inHeliconius melpomene

Byers

Darragh

Musgrove

et al. 2019

Preprint

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Understanding the production, response, and genetics of signals used in mate choice can inform our understanding of the evolution of both intraspecific mate choice and reproductive isolation. Sex pheromones are important for courtship and mate choice in many insects, but we know relatively little of their role in butterflies. The butterfly Heliconius melpomene uses a complex blend of wing androconial compounds during courtship. Electroantennography in H. melpomene and its close relative Heliconius cydno showed that responses to androconial extracts were not species specific. Females of both species responded equally strongly to extracts of both species, suggesting conservation of peripheral nervous system elements across the two species. Individual blend components provoked little to no response, with the exception of octadecanal, a major component of the H. melpomene blend. Supplementing octadecanal on the wings of octadecanal-rich H. melpomene males led to an increase in the time until mating, demonstrating the bioactivity of octadecanal in Heliconius. Using quantitative trait locus (QTL) mapping, we identified a single locus on chromosome 20 responsible for 41% of the parental species' difference in octadecanal production. This QTL does not overlap with any of the major wing color or mate choice loci, nor does it overlap with known regions of elevated or reduced F ST . A set of 16 candidate fatty acid biosynthesis genes lies underneath the QTL. Pheromones in Heliconius carry information relevant for mate choice and are under simple genetic control, suggesting they could be important during speciation. K E Y W O R D S : Behavior, electroantennography, Heliconius, pheromones, quantitative trait locus mapping.

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“…Furthermore, we uncovered an evolutionary mechanism, gene duplication followed by neofunctionalization and subfunctionalization, by which ITC-responsive Ors evolved in Brassicales specialists. More generally, our results suggest that major host shifts and specialization events in herbivorous insects can result from relatively simple genetic changes of large effect on the peripheral nervous system, similar to the apple maggot fly Rhagoletis pomonella (45). This in turn may explain why such events are so common across herbivorous insect lineages, resulting in rapid rates of diversification and leading to the most diverse guild of macroscopic life (46,47).…”

Section: Discussionmentioning

confidence: 62%

Evolution of olfactory receptors tuned to mustard oils in herbivorous Drosophilidae

Matsunaga

Reisenman

Goldman-Huertas

et al. 2019

Preprint

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248): 21 Plant toxins are effective defenses because they are aversive to most insects. The same 22 molecules, however, are co-opted as host-finding cues by specialist herbivores. Although such 23 behavioral shifts are central to our understanding of herbivorous insect diversification, it is not 24 well understood how these behaviors evolve. We addressed this in Scaptomyza flava, a 25 herbivorous drosophilid fly within a lineage that shifted to feeding on toxic mustard plants 26 (Brassicales) less than 10 million years ago. S flava lost the ancestral attraction to yeast volatiles 27 and the attendant chemoreceptors used to detect these odors. Here we report that S. flava, but not 28 its close microbe-feeding relatives Drosophila melanogaster and S. pallida, is attracted to 29 mustard host-plant odors, including volatile mustard oils (isothiocyanates or ITCs). Our genomic 30 analysis uncovered three S. flava paralogs of an olfactory receptor gene (Or67b) that likely 31 experienced recent positive selection. We then tested whether these chemoreceptors could 32 underlie the observed attraction to volatile ITCs. Our in vivo recordings revealed that two of the 33 S. flava Or67b proteins (Or67b1 and Or67b3) -but not the homologous Ors from microbe-34 feeding relatives -responded selectively and sensitively to volatile ITCs. These Ors are the first 35 ITC chemoreceptors other than TRP channel family (e.g., the TrpA1 'wasabi' receptor) known 36 from any animal. Remarkably, S. flava Or67b3 was sufficient to drive olfactory attraction toward 37 butyl ITC when expressed in an attractive olfactory circuit. Our study illuminates that ancestrally 38 aversive chemicals can be co-opted as attractants through gene duplication, leading to the origin 39 of hedonic valence shifts in herbivorous insects. 40 41 42Significance Statement (120) 43 Plant toxins trigger aversive olfactory (volatile-mediated) and gustatory (contact-mediated) 44 responses in animals. Paradoxically, toxic plants are often colonized by specialist insects that co-45 opt these toxins as host-plant finding cues. The mechanisms underlying these behavioral shifts, 46 from indifference or repulsion to plant chemicals, to attraction, remain unclear. To address this, 47 we used a fly lineage, Scaptomyza, that switched from yeast-feeding to feeding on mustard plants 48 less than 10 million years ago. We found that S. flava is attracted to mustard-plant odors and 49 volatile mustard oils (isothiocyanates or ITCs) such as 'wasabi', a behavior enabled by the 50 evolution of genes encoding odorant receptors highly sensitive to ITCs. Our study illuminates 51 how insects colonize toxic host plants through duplication and ecological repurposing of genes 52 encoding pre-existing chemoreceptors. 53 54 55 56 57 Many plant compounds used in food, agriculture and medicine originally evolved as 58 toxins that deter and repel enemies (1). Among the most well-known compounds are those 59 reactive electrophiles that induce the sensation of pain, such as diallyl disulfide a...

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Sensory specificity and speciation: a potential neuronal pathway for host fruit odour discrimination in Rhagoletis pomonella

Cited by 31 publications

References 53 publications

A major locus controls a biologically active pheromone component inHeliconius melpomene

A major locus controls a biologically active pheromone component inHeliconius melpomene

A major locus controls a biologically active pheromone component inHeliconius melpomene

Evolution of olfactory receptors tuned to mustard oils in herbivorous Drosophilidae

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