Biology subjects

Dion, E.

Publications and source records attributed to Dion, E..

4 recordsLinked to original sources

bioRxiv2024

Butterfly brains change in morphology and in gene splicing patterns after brief pheromone exposure

How insect brains differ between the sexes and respond to sex-specific pheromones is still not well understood. Here we briefly exposed female Bicyclus anynana butterflies to wild type (Wt) and modified male sex pheromone blends, previously shown to modify females sexual preferences, and examined how their brains were modified at the morphological and molecular levels, three days later. First, we 3D-reconstructed male and female brains of this species and documented sexual dimorphism in the size of seven of 67 glomeruli present in the olfactory lobe. Then we showed that several glomeruli changed in volume after blend exposures, implicating them in sex pheromone perception. Finally, we found that a few genes were differentially expressed but many more were differentially spliced between male and female naive brains, and between naive and pheromone blend-exposed brains. These are primarily calcium-binding channels and RNA-binding genes, respectively. A learned preference for changed levels in a single pheromone component was linked to variants of proteins involved in synaptic transmission. Our work shows that naive male and female brains differ primarily in gene splicing patterns and that a brief, 3-minute, exposure to pheromones produces slight changes in brain volume and large changes in the splicing of genes involved in neural development, that correlate with changes in sexual preferences in females. Significance statementHow brains differ between the sexes and respond to sex-specific cues is a hot research topic. Here we investigate how the brains of female butterflies differ from those of males and respond to male sex pheromones. We find that the sexes differ in the volume of a sub-set of olfactory lobe glomeruli, and the volume of some glomeruli also changes after exposure to pheromone blends. In addition, male and female brains differ primarily in hundreds of splice variants, both before and after pheromone exposure. These findings suggest that different proteins (splice variants) characterize male and female brains and that a brief exposure to pheromones can lead to changes in brain structure and in further gene splicing linked to altered sexual preferences in female butterflies.

animal behavior and cognition↗

bioRxiv2023

The molecular basis of macrochaete diversification highlighted by a single-cell atlas of Bicyclus anynana butterfly pupal forewings

Butterfly wings display a large diversity of cell types, including scale cells of different colors, shapes, and sizes, yet the molecular basis of such diversity is poorly understood. Scales are single-cellular projections homologous to sensory bristles in other arthropods, and different scale types are often found intermingled on the wing, alongside other sensory and epidermal cell types, making the analysis of the complete transcriptomes of each scale type difficult to achieve. To explore scale cell diversity at a transcriptomic level we employed single-cell RNA sequencing of [~]5200 large cells (>6 {micro}m) from 22.5-25-hour male pupal forewings of the butterfly Bicyclus anynana. Using single-cell unsupervised, transcriptome clustering, based on shared and differentially expressed genes, followed by in situ hybridization, immunofluorescence, and CRISPR/Cas9 editing of candidate cell type specific genes, we annotate various cell types on the wing. We identify the molecular identities of non-innervated scale cells at various stages of differentiation, innervated sensory cell types, and pheromone producing glandular cells. We further show that senseless, a zinc finger transcription factor, and HR38, a hormone receptor, determine the identity, size, and color of different scale cell types and are important regulators of scale cell differentiation. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=100 SRC="FIGDIR/small/554425v1_ufig1.gif" ALT="Figure 1"> View larger version (29K): org.highwire.dtl.DTLVardef@10624org.highwire.dtl.DTLVardef@13a4963org.highwire.dtl.DTLVardef@1a83a9borg.highwire.dtl.DTLVardef@19f9d1e_HPS_FORMAT_FIGEXP M_FIG C_FIG

developmental biology↗

bioRxiv2021

Developmental plasticity in male courtship in Bicyclus anynana butterflies is driven by hormone regulation of the yellow gene

The organizational role for hormones in the regulation of sexual behavior is currently poorly explored. Previous work showed that seasonal variation in levels of the steroid hormone 20-hydroxyecdysone (20E) during pupal development regulates plasticity in male courtship behavior in Bicyclus anynana butterflies. Wet season (WS) males, reared at high temperature, have high levels of 20-hydroxyecdysone (20E) during pupation and become active courters. Dry season (DS) males, reared at low temperatures, have lower levels of 20E and lower courtship rates. Rescue of WS courtship rates can be achieved via injection of 20E into DS male pupae, but it is still unknown whether 20E alters gene expression in the pupal brain, and if so, the identity of those targets. Using transcriptomics, qPCR, and behavioral assays with a transgenic knockout, we show that higher expression levels of the yellow gene in DS male pupal brains, relative to WS brains, represses courtship in DS males. Furthermore, injecting DS males with 20E downregulates yellow to WS levels 4 hours post-injection, revealing a hormone sensitive window that determines courtship behavior. These findings are in striking contrast to Drosophila, where yellow is required for active male courtship behavior. We conclude that 20E plays an organizational role during pupal brain development by regulating the expression of yellow, which is a repressor of the neural circuity for male courtship behavior in B. anynana. This work shows that similar to vertebrates, hormones can also play an organizational role in insect brains, leading to permanent changes in adult sexual behavior. Significance StatementBehavioral plasticity in adult insects is known to be regulated by hormones, which activate neural circuits in response to environmental cues. Here, we show that hormones can also regulate adult behavioral plasticity by altering gene expression during brain development, adjusting the insects behavior to predictable seasonal environmental variation. We show that seasonal changes in the hormone 20E alters expression of the yellow gene in the developing pupal brain of Bicyclus anynana butterflies, which leads to differences in male courtship behavior between the dry and wet seasonal forms. This work provides one of the first examples of the organizational role of hormones in altering gene expression and adult sexual behavior in the developing insect brain.

neuroscience↗

bioRxiv2017

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

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 naive offspring of females that underwent distinct odor learning trials to test for a potential inheritance of learned odor preferences. Naive (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. Naive 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.\n\nSignificance 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.

evolutionary biology↗