bioRxiv Science⌕ Search

bioRxiv · 10.1101/2024.10.02.615994

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

Abstract

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.

Source connections

Explore related subjects

Keep this discovery

Explore connections, maps & timelines

BibTeXRIS

Dion, E., Toh, Y. P., Zhu, D., Monteiro, A.. 2024-10-03. Butterfly brains change in morphology and in gene splicing patterns after brief pheromone exposure. https://doi.org/10.1101/2024.10.02.615994

Cite the original work for its findings. Save a collection to share your selection of sources.

KEEP EXPLORING

Related preprints

Deconstructing Boldness: Latent behavioural structure across novelty, predation, and exploration in an endangered species translocation program

Risk-related behaviours including neophobia, exploration, and predator avoidance are often assumed to covary along a general boldness axis. Although some translocation studies have linked one or more of these behaviours with fitness, it is possible that the underlying behavioural structure varies under different selective environments. Conservation breeding programs provide a unique opportunity to evaluate the structure of behavioural correlations in a non-domestic species under artificial conditions. We tested whether risk-related behaviours represent a unified boldness syndrome in a captive population of the endangered Attwaters prairie chicken (APC; Tympanuchus cupido attwateri). We quantified the repeatable behaviours of 257 juveniles and compared 11 models of behavioural covariation structure using multivariate mixed models and confirmatory factor analysis. There was no support for a single risk-taking axis; instead, we found three dimensions representing responses to novelty and environmental stimuli (Engagement), predator avoidance (Threat Response), and maze exploration (Maze Progression). Our results indicate that these risk-related behaviours are not organized along a single axis in captive APCs, challenging assumptions that risk-taking represents a universal behavioural syndrome. To anticipate post-release success accurately, conservation managers should understand the exact behavioural architecture of the captive population rather than assume that the classical bold-shy structure occurs in all contexts.

animal behavior and cognition↗

Social costs of group life: Larger groups have less affiliative behavior and more social conflict

The costs and benefits of sociality depend in part upon the size of groups. Therefore, individual behavior should vary across groups of different sizes, reflecting group size-dependent costs and benefits. Here, we test this prediction using a long-term dataset on wild female baboons (Papio cynocephalus x P. anubis). We find that individuals who live in larger groups suffer social costs: compared to animals in smaller groups, they experience more agonistic interactions, fewer grooming interactions, and sparser social networks. These social costs arise, in part, from a pattern in which relationships within dyads become more agonistic as group size increases (i.e., a given dyad exhibits fewer grooming interactions relative to agonistic interactions when it is living in a larger group). While individuals in large groups generally maintain the same number of strong bonds as individuals in small groups, they tend to develop weak bonds with a greater number of social partners that results in, on average, weaker bonds overall. Our results demonstrate that, despite potential benefits to large groups in terms of predation risk and intergroup competition, the social lives of individuals in larger groups involve less affiliation and more conflict in this wild primate population.

animal behavior and cognition↗

Shared brain transcriptome signatures of social evolution and plasticity in shell-dwelling cichlid fishes

Inter-individual variability in phenotypic traits is widespread in nature both across and within species, with similar patterns of variation often occurring between and within species. Given that these two types of variation are generated by evolutionary and plasticity processes respectively, it raises the question to what extent the causal mechanisms underlying such variability at these two different levels are shared or not. To address this question, we studied the variation in brain transcriptomes in Tanganyikan cichlids that exhibit both intra- and interspecific variation in social behavior. We compared two facultatively social cichlid species, each containing naturally occurring solitary and social-living individuals, with a closely related obligatory solitary resembling the ancestral state. Differential gene expression and Gene Set Enrichment Analyses were performed in the telencephalon and diencephalon transcriptomes to investigate the molecular basis of both behavioral plasticity and the evolution of sociality. Behavioral plasticity involved few differentially expressed genes but extensive changes in biological pathways, supporting a highly polygenic architecture of social behavior. Across both species, social-living individuals consistently upregulated pathways involved in translation, protein homeostasis, and energy metabolism, whereas solitary individuals showed enrichment of neuronal morphogenesis, cell adhesion, and structural plasticity. Remarkably, these same functional programs were associated with the independent evolution of sociality, revealing a strong overlap between evolutionary and plastic transcriptional responses. This convergence was largely restricted to the telencephalon, while the diencephalon showed limited and inconsistent functional signatures. Together, our results support the repeated recruitment of gene regulatory programs during the evolution of sociality and demonstrate that behavioral plasticity and evolutionary transitions share common neurogenomic responses, consistent with a conserved genetic toolkit for social behavior.

animal behavior and cognition↗