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Biology subjects

Toh, Y. P.

Publications and source records attributed to Toh, Y. P..

4 recordsLinked to original sources

Adaptation in the eye and brain contributes to species divergence in visual perception in Heliconius butterflies

Sensory systems mediate the interaction between organisms and their environment, but how complex sensory pathways evolve and relate to variation in perception and behavior across ecological contexts, remains poorly understood, especially for terrestrial taxa. Here, we investigate whole-visual-system adaptation in Heliconius erato butterflies. Using continent-wide sampling, we demonstrate that within H. erato, facet count significantly decreased with increasing elevation. Common-garden rearing of low-elevation H. erato populations from Ecuador and their high-elevation sister species, H. himera, showed that eye and brain morphology are heritable, and comparisons to genomic measures of divergence indicates that this variation is due to divergent selection. Parallel comparisons from Colombia involving H. chestertonii (high elevation) and H. erato venus (low elevation) further revealed that eye and brain morphology can evolve as independent, decoupled traits. For both locations, differences in visual acuity correlated with variation in facet count. We also observed parallel evolution of spectral sensitivity, with independent high-elevation populations having fewer red-reflecting lateral filtering pigments. To experimentally link visual system morphology to behavior, we assessed visual acuity in second-generation H. erato cyrbia-H. himera hybrids. Overall, acuity was influenced by facet count, and when analyzed together with brain morphology, by a positive interaction between facet count and optic lobe volume, demonstrating that structural investment in the eye and neural expansion combine to maximize visual perception. This work shows that visual adaptation is a multi-layered process whereby sensory traits can evolve independently under localized ecological pressures, but evolution across the visual pathway contributes to refinements in behavioral performance.

evolutionary biology↗

Distinct evolutionary trajectories of two integration centres, the central complex and mushroom bodies, across Heliconiini butterflies

Neural circuits have evolved to produce cognitive processes that facilitate a species variable behavioural repertoire. Underlying this variation are evolutionary forces, such as selection, that operate on changes to circuitry against a background of constraints. The interplay between selection and potentially limiting constraints determine how circuits evolve. Understanding how this process operates requires an evolutionary framework that facilitates comparative analysis of neural traits, within a clear behavioural and functional context. We leverage a large radiation of Heliconiini butterflies to examine how selection shapes the evolution of the central complex and the mushroom bodies, two integration centres in the insect brain involved in spatial navigation. Within the Heliconiini, one genus, Heliconius, performs systematic spatial foraging and navigation to exploit specific plants as a source of pollen, a novel dietary resource. Closely related genera within Heliconiini lack this dietary adaptation, and are more vagrant foragers. The evolution of increased spatial fidelity in Heliconius has led to changes in brain morphology, and in specific learning and memory profiles, over a relatively short evolutionary time scale. Here, using a dataset of 41 species, we show that in contrast to a massive expansion of the mushroom bodies, the central complex and associated visual processing areas are strongly conserved in size and general architecture. We corroborate this by characterising patterns of fine anatomical conservation, including conserved patterns in dopamine and serotonin expression. However, we also identify a divergence in the expression of a neuropeptide, Allatostatin A, in the noduli, and in the numbers of GABA-ergic ellipsoid body ring neurons and their branching in the fan-shaped body, which are essential members of the anterior compass pathway. These differences match expectations of where evolutionary adaptability might occur inside the central complex network and provide rare examples of divergence of these circuits in a shallow phylogenetic context. We conclude that due to the contrasting volumetric conservation of the central complex and the massive volumetric differences in the mushroom bodies, their circuit logics must determine distinct responses to selection associated with divergent foraging behaviours.

neuroscience↗

Evolution of the olfactory system during the radiation of Heliconiini butterflies

Sensory system evolution plays a crucial role in shaping species interactions with their environment, yet the extent to which olfactory system diversity reflects ecological and evolutionary pressures at a macroevolutionary scale remains unclear. Here, we investigate the evolution of the olfactory system across the Heliconiini butterfly tribe, an ecologically diverse but closely related group. Using a comparative approach, we examined variation in antennal lobe morphology and its constituent structures, the glomeruli and antennal lobe hub, as well as olfactory receptor repertoires across species. We found that antennal lobe size variation is driven by independent shifts in glomerular and antennal lobe hub volumes, with species-specific differences occurring against a backdrop of broader phylogenetic stability. While no direct associations with ecological traits were observed, certain species showed large expansions in total glomerular volume and olfactory receptor numbers, warranting further investigation into unmeasured ecological or behavioural factors. Additionally, comparisons between wild-caught and insectary-reared individuals revealed a surprising pattern of developmental plasticity, with antennal lobe hub volumes increasing and glomeruli volumes decreasing in captivity, highlighting the influence of environmental conditions on neural development. These findings suggest that olfactory evolution in Heliconiini is shaped by both evolutionary divergence and developmental plasticity, emphasizing the need to integrate phylogenetic, ecological, and developmental perspectives to fully understand sensory system adaptation.

evolutionary biology↗

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↗