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Young, F. J.

Publications and source records attributed to Young, F. J..

6 recordsLinked to original sources

Cognitive robustness in a new insect model of extended longevity

Human life expectancy has jumped by several decades in the last century, but the healthspan has not followed suit. The ageing population has come with an increased prevalence of neurodegenerative disease, and insects have proven to be valuable models of these conditions and their associated cognitive decline. The Heliconius butterfly genus is an emerging system in insect cognition, having recently evolved a significant expansion in neural centres of learning and memory, alongside enhanced stability of visual long-term memory in comparison with their close relatives in the Heliconiini tribe. This is linked to the cognitive demands imposed by Heliconius spatially-faithful foraging behaviour for a protein-rich diet of pollen, and co-occurs with a dramatic lifespan extension in this genus over the other Heliconiini outgroups. Here, we investigate whether the Heliconius cognitive healthspan is similarly discrepant, or if any cognitive decline is instead delayed in accordance with their lifespan extension. We first report evidence that investment in learning and memory circuits co-evolves with Heliconiini lifespan. We then conduct learning and memory assays across the lifespans of a representative longer-lived Heliconius, H. hecale, and the shorter-lived Heliconiini outgroup, Dryas iulia. Across both species, and particularly in H. hecale, we find evidence for cognitive robustness in late life, in contrast to evidence for widespread cognitive declines in insects. Our results add a new taxonomic order to the study of age-related memory impairment, and suggest Heliconius as a valuable model system for mechanistic studies of the maintenance of neurological health in the context of extended life.

animal behavior and cognition↗

Evolution of increased longevity and slowed ageing in a genus of tropical butterfly

Evolution has given rise to lifespans in extant species ranging from days to centuries. Given that mechanisms of ageing are highly conserved, studying long-lived lineages across the animal kingdom could yield insights relevant for healthy ageing in humans. However, typical models of extended lifespan often live for decades, making them impractical for longitudinal studies. Ideal model systems would be organisms that are naturally long-lived compared to their close relatives, but have lifespans on experimentally tractable scales. Here, we present the Neotropical butterfly genus Heliconius as a novel model system for the evolution of extended longevity. We collate data from 27 species across the Heliconiini tribe to reveal a 25-fold variation in lifespan within the group, with our 348-day maximum for Heliconius hewitsoni longer than any butterfly species previously recorded in the scientific literature. While previous work has attributed this lifespan extension to a plastic response to enhanced nutrition, we conduct detailed survival and functional senescence analyses on two species representative of shorter- and longer-lived clades to show evidence of evolved, heritable mechanisms of slowed ageing in Heliconius. Our results add a new case study to the canon of noteworthy agers, and provide valuable insights into the evolution of increased longevity.

evolutionary biology↗

Enhanced long-term memory and increased mushroom body plasticity in Heliconius butterflies

As highly labile structures on both individual and evolutionary time-scales, the mushroom bodies, a key site of learning and memory in insects, are an excellent model for investigating the evolution of cognitive variation. We explored the behavioural consequences of mushroom body expansion in Heliconius butterflies, which possess greatly expanded mushroom bodies relative to their closest outgroups. We conducted long-term visual memory assays across three Heliconius and three other Heliconiini species using trained food-colour associations. We confirm robust differences between clades, with Heliconius exhibiting greater fidelity to the trained colour after 8 days without reinforcement compared to other Heliconiini, with further evidence of stable preferences at 13 days. We extended this analysis to consider the plastic response of the mushroom body calyces over this time period, measuring the volume of the mushroom body calyx, and the number of neurons and synapses it contains. We find substantial post-eclosion expansion and synaptic pruning in calyx of Heliconius erato, but not in Dryas iulia. In Heliconius erato, visual associative learning experience specifically is associated with a greater retention of calyceal synapses. At an individual level, fidelity to the trained colour in Heliconius erato was also positively correlated with synapse number. These results point to an enhanced visual long-term memory across Heliconius, facilitated not only by phylogenetic expansion of the mushroom body, but also changes in its developmental response to learning experience. The co-evolution of mushroom body expansion, plasticity and specific behaviours provides an important case study in the evolution of cognition. Significance StatementHow are cognitive differences between species supported by evolutionary changes in the brain? We investigated this question using Heliconius butterflies which have expanded mushroom bodies, a region of the insect brain involved in learning and memory. We show that Heliconius have more stable visual long-term memories and exhibit more substantial age- and experience-related plasticity than a closely related genus with smaller mushroom bodies. Recall accuracy was also predicted by synapse number in Heliconius erato, but not Dryas iulia, suggesting functional importance. These results suggest that increases in the size of specific brain regions and changes in their plastic response to experience may co-evolve to shape the evolution of cognition.

animal behavior and cognition↗

Reversal learning of visual cues in Heliconiini butterflies

The mushroom bodies, an integrative region of the insect brain involved in learning and memory, have undergone volumetric increase in several independent lineages includes bees and ants, cockroaches and some beetles. However, the selective pressures driving these expansion events are not fully understood. One promising system for investigating this question is the Neotropical butterfly genus Heliconius, which exhibits markedly enlarged mushroom bodies compared with other members of the Heliconiini tribe. Notably, this neural elaboration co-occurs with the evolution of trapline foraging behaviour and an improved capacity for learning complex visual cues and long-term memory. Here, we further investigate the behavioural consequences of this brain expansion by testing reversal learning ability, a commonly used measure of cognition and behavioural flexibility in both vertebrates and invertebrates, across three Heliconius and three closely-related Heliconiini species. We trained butterflies to associate a food reward with either purple or yellow flowers, before training them with the reversed associations, and then reversing the cues again. All six successfully learned the reversed cues, and, contrary to our expectations, we found no evidence that Heliconius performed better than the other Heliconiini species. These results are surprising, given previous evidence linking the mushroom bodies to reversal learning in other insects, and the enhanced performance of Heliconius in other cognitive tests. This serves as a reminder that the functional consequences of brain expansion can be multifaceted, and do not necessarily result in an overall increase in general cognitive ability, but rather enhanced performance in specific, ecologically-relevant tasks.

animal behavior and cognition↗

Rapid expansion and visual specialization of learning and memory centers in Heliconiini butterflies

How do neural systems evolve to support new behaviors? Changes in the abundance and diversity of neural cell types, and their connectivity, shape brain composition and provide the substrate for behavioral variation. We describe a striking example of neural elaboration in an ecologically diverse tribe of Heliconiini butterflies. By building extensive new datasets of neural traits across the tribe, we identify major bursts in the size and cellular composition of the mushroom bodies, central brain structures essential for learning and memory. These expansion events are associated with increased innervation form visual centers and coincide with enhanced performance in multiple cognitive assays. This suite of neural and cognitive changes is likely tied to the emergence of derived foraging behaviors, facilitated by localized specialization of neural networks. One-Sentence SummaryMajor shifts in brain composition and behavior in butterflies with unique foraging and dietary behaviors.

evolutionary biology↗

Heliconiini butterflies can learn time-dependent reward associations

For many pollinators, flowers provide predictable temporal schedules of resource availability, meaning an ability to learn time-dependent information could be widely beneficial. However, this ability has only been demonstrated in a handful of species. Observational studies of Heliconius butterflies suggest that they may have an ability to form time-dependent foraging preferences. Heliconius are unique among butterflies in actively collecting and digesting pollen, a dietary behaviour linked to spatiotemporally faithful ‘trap-line’ foraging. Time-dependency of foraging preferences is hypothesised to allow Heliconius to exploit temporal predictability in alternative pollen resources, as well as contributing to optimal use of learnt foraging routes. Here, we provide the first experimental evidence in support of this hypothesis, demonstrating that Heliconius hecale can learn opposing colour preferences in two time periods. This shift in preference is robust to the order of presentation, suggesting that preference is tied to the time of day and not due to ordinal learning. However, we also show that this ability is not limited to Heliconius, as previously hypothesised, but is also present in a related genus of non-pollen feeding butterflies. This demonstrates that time learning pre-dates the origin of pollen-feeding and may be prevalent across butterflies with less specialized foraging behaviours.Competing Interest StatementThe authors have declared no competing interest.View Full Text

animal behavior and cognition↗