Biology subjects

Farnworth, M. S.

Publications and source records attributed to Farnworth, M. S..

7 recordsLinked to original sources

bioRxiv2025

Conservation of sensory pathways implies a localised change in the mushroom bodies is associated with cognitive evolution in Heliconius butterflies

Acquisition of novel behaviour is reflected in changes in sensory investment or integration, but the exact nature of these changes is often unclear. Within the Neotropical butterfly tribe, Heliconiini, the genus Heliconius possess 4-fold larger mushroom bodies, an insect learning and memory centre, than closely related Heliconiini. Mushroom body expansion in Heliconius co-occurred with a dietary innovation, and is associated with systematic spatial foraging and extended lifespans. Heliconiini therefore offer an attractive system for studying how behavioural evolution is facilitated by changes in neural systems. Heliconius foraging relies on visual scene memories and, indeed, Heliconius have more stable visual long-term memory, and evidence of visual specialisation in the mushroom bodies. Here, we explore how vision-specific neuroanatomical and behavioural enhancement in Heliconius impacts sensory pathways upstream of the mushroom bodies by assessing investment across the eyes, sensory structures and projection pathways. Despite evidence of refinement in visually-based behaviour, we found no increased investment in visual structures, brain areas or pathways. This suggests that the rapid expansion of the Heliconius mushroom body occurred in a context of conserved detection and processing of visual cues, and that a localised shift within integrative brain centres facilitated the evolution of Heliconius novel behaviours.

evolutionary biology↗

bioRxiv2025

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↗

bioRxiv2024

Modality specific memory enhancement in Heliconius butterflies

How animals perceive, process and respond to environmental cues is tightly tuned to the species-specific demands, and reflected by the structure of neural systems. In the Neotropical butterflies, Heliconius, the mushroom bodies, insect learning and memory centres, are significantly expanded compared to their closest relatives. This expansion coincided with the evolution of a novel diet, pollen feeding, and a spatial foraging behaviour consistent with trap-lining. Previous research has shown that Heliconius have more accurate visual long-term memory than other Heliconiini. Here, we tested whether this enhanced memory stability is specific to visual cues by conducting a long-term olfactory memory assay in two Heliconius species and two outgroup species. We found no differences in the long-term olfactory memory between Heliconius species and the outgroup species. Combining data from olfactory and visual memory trials confirms a significant shift in performance among sensory modalities between Heliconius and outgroup genera. In contrast, tests of how Heliconiini prioritise olfactory and visual cues when in presented in conflict also show no consistent shift in attentiveness to sensory cues between species. Our data provide a rare case where memory performance has been compared across species and sensory modalities, to identify evidence of a modality specific shift.

animal behavior and cognition↗

bioRxiv2024

Mosaic evolution of a learning and memory circuit in Heliconiini butterflies

A critical function of central neural circuits is to integrate sensory and internal information to cause a behavioural output. Evolution modifies such circuits to generate adaptive change in sensory detection and behaviour, but it remains unclear how selection does so in the context of existing functional and developmental constraints. Here, we explore this question by analysing the evolutionary dynamics of insect mushroom body circuits. Mushroom bodies are constructed from a conserved wiring logic, mainly consisting of Kenyon cells, dopaminergic neurons and mushroom body output neurons. Kenyon cells carry sensory identity signals, which are modified in strength by dopaminergic neurons and carried forward into other brain areas by mushroom body output neurons. Despite the conserved makeup of this circuit, there is huge diversity in mushroom body size and shape across insects. However, an empirical framework of how evolution modifies the function and architecture of this circuit is largely lacking. To address this, we leverage the recent radiation of a Neotropical tribe of butterflies, the Heliconiini (Nymphalidae), which show extensive variation in mushroom body size over comparatively short phylogenetic timescales, linked to specific changes in foraging ecology, life history and cognition. To understand the mechanism by which such an extensive increase in size is accommodated through changes in lobe circuit architecture, we first combined immunostainings of structural markers, neurotransmitters and neural injections to generate, to our knowledge, the most detailed description of a Papilionoidea butterfly mushroom body lobe. We then provide a comparative, quantitative dataset which shows that some Kenyon cell populations expanded with a higher rate than others in Heliconius, providing an anatomical parallel to specific shifts in behaviour. Finally, we identified an increase in GABA-ergic feedback neurons essential for non-elemental learning and sparse coding, but conservation in dopaminergic neuron number. Taken together, our results demonstrate mosaic evolution of functionally related neural systems and cell types and identify that evolutionary malleability in an architecturally conserved parallel circuit guides adaptation in cognitive ability.

evolutionary biology↗

bioRxiv2021

An atlas of the developing Tribolium castaneum brain reveals conserved anatomy and divergent timing to Drosophila melanogaster

Insect brains are formed by conserved sets of neural lineages whose fibres form cohesive bundles with characteristic projection patterns. Within the brain neuropil these bundles establish a system of fascicles constituting the macrocircuitry of the brain. The overall architecture of the neuropils and the macrocircuitry appear to be conserved. However, variation is observed e.g., in size and shape and timing of development. Unfortunately, the developmental and genetic basis of this variation is poorly understood although the rise of new genetically tractable model organisms such as the red flour beetle Tribolium castaneum allows the possibility to gain mechanistic insights. To facilitate such work, we present an atlas of the developing brain of T. castaneum, covering the first larval instar, the prepupal stage and the adult, by combining wholemount immunohistochemical labelling of fibre bundles (acetylated tubulin) and neuropils (synapsin) with digital 3D reconstruction using the TrakEM2 software package. Upon comparing this anatomical dataset with the published work in D. melanogaster, we confirm an overall high degree of conservation. Fibre tracts and neuropil fascicles, which can be visualized by global neuronal antibodies like anti-acetylated tubulin in all invertebrate brains, create a rich anatomical framework to which individual neurons or other regions of interest can be referred to. The framework of a largely conserved pattern allowed us to describe differences between the two species with respect to parameters such as timing of neuron proliferation and maturation. These features likely reflect adaptive changes in developmental timing that govern the change from larval to adult brain.

neuroscience↗

bioRxiv2019

Sequence heterochrony led to a gain of functionality in an immature stage of the central complex: a fly-beetle insight

Animal behavior is guided by the brain. Therefore, adaptations of brain structure and function are essential for animal survival, and each species differs in such adaptations. The brain of one individual may even differ between life stages, for instance as adaptation to the divergent needs of larval and adult life of holometabolous insects. All such differences emerge during development but the cellular mechanisms behind the diversification of brains between taxa and life stages remain enigmatic. In this study, we investigated holometabolous insects, where larvae differ dramatically from the adult in both behavior and morphology. As consequence, the central complex, mainly responsible for spatial orientation, is conserved between species at the adult stage, but differs between larvae and adults as well as between larvae of different taxa. We used genome editing and established transgenic lines to visualize cells expressing the conserved transcription factor retinal homeobox, thereby marking homologous genetic neural lineages in both the fly Drosophila melanogaster and the beetle Tribolium castaneum. This approach allowed us for the first time to compare the development of homologous neural cells between taxa from embryo to the adult. We found complex heterochronic changes including shifts of developmental events between embryonic and pupal stages. Further, we provide, to our knowledge, the first example of sequence heterochrony in brain development, where certain developmental steps changed their position within the ontogenetic progression. We show that through this sequence heterochrony, an immature developmental stage of the central complex gains functionality in Tribolium larvae. We discuss the bearing of our results on the evolution of holometabolous larval central complexes by regression to a form present in an ancestor.

evolutionary biology↗

bioRxiv2019

An ancestral apical brain region contributes to the central complex under the control of foxQ2 in the beetle Tribolium castaneum

The genetic control of anterior brain development is highly conserved throughout animals. For instance, a conserved anterior gene regulatory network specifies the ancestral neuroendocrine center of animals and the apical organ of marine organisms. However, its contribution to the brain in non-marine animals has remained elusive. Here, we study the function of the Tc-foxQ2 forkhead transcription factor, a key regulator of the anterior gene regulatory network of insects. We characterized four distinct types of Tc-foxQ2 positive neural progenitor cells based on differential co-expression with Tc-six3/optix, Tc-six4, Tc-chx/vsx, Tc-nkx2.1/scro, Tc-ey, Tc-rx and Tc-fez1. An enhancer trap line built by genome editing marked Tc-foxQ2 positive neurons, which projected through the primary brain commissure and later through a subset of commissural fascicles. Eventually, they contributed to the central complex. Strikingly, in Tc-foxQ2 RNAi knock-down embryos the primary brain commissure did not split and subsequent development of midline brain structures stalled. Our work establishes foxQ2 as a key regulator of brain midline structures, which distinguish the protocerebrum from segmental ganglia. Unexpectedly, our data suggest that the central complex evolved by integrating neural cells from an ancestral anterior neuroendocrine center.\n\nSummary statementAn ancestral neuroendocrine center contributes to the evolution of the central complex. foxQ2 is a gene required for the development of midline structures of the insect brain, which distinguish protocerebrum from segmental ganglia.

developmental biology↗