Linking ecological specialisation to adaptations in butterfly brains and sensory systems

Couto, Antoine; Wainwright, J. Benito; Morris, Billy J.; Montgomery, Stephen H.

doi:10.1016/j.cois.2020.09.002

Cited by 21 publications

(19 citation statements)

References 49 publications

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“…This includes classic work characterising pheromones, the olfactory response to these chemical cues, and the manner in which the pheromone processing system evolves (Butenandt et al 1959; Klun and Maini, 1979; Namiki et al 2014). Studies on lepidopteran sensory systems have provided crucial insights into how sensory systems function, how separate strands of information are processed and integrated within the brain, and the relationship between sensory systems and ecological variables (Couto et al 2020).…”

Section: Introductionmentioning

confidence: 99%

Re-emergence and diversification of a specialised antennal lobe morphology in ithomiine butterflies

Morris

Couto

Aldin³

et al. 2020

Preprint

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How an organisms sensory system functions is central to how it navigates its environment and meets the behavioural challenges associated with survival and reproduction. Comparing sensory systems across species can reveal how facets of behaviour and ecology promote adaptive shifts in the relative importance of certain environmental cues. The insect olfactory system is prominent model for investigating how ecological factors impact sensory reception and processing. Notably work in Lepidoptera led to the discovery of vastly expanded structures, termed a macroglomerular complex (MGC), within the primary olfactory processing centre. These structures typically process pheromonal cues and provide a classic example of how variation in size can influence the functional processing of sensory cues. Though prevalent across moths, the MGC was lost during the early evolution of butterflies, consistent with evidence that courtship initiation in butterflies is primarily reliant upon visual cues, rather than long distance olfactory signals like pheromones. However, a MGC has recently been reported to be present in a species of ithomiine, Godryis zavaleta, suggesting this once lost neural adaptation has re-emerged in this clade. Here, we show that MGCs, or MGC-like morphologies, are indeed widely distributed across the ithomiine tribe, and vary in both structure and the prevalence of sexual dimorphism. Based on patterns of variation across species with different chemical ecologies, we suggest that this structure is involved in the processing of both plant and pheromonal cues, of interlinked chemical constitution, and has evolved in conjunction with the increased importance and diversification of plant derived chemicals cues in ithomiines.

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Section: Introductionmentioning

confidence: 99%

Re-emergence and diversification of a specialised antennal lobe morphology in ithomiine butterflies

Morris

Couto

Aldin³

et al. 2020

Preprint

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“…Across Lepidoptera, the neuroanatomical structures that process sensory information are well conserved, but the relative volume of individual brain structures, or neuropils, varies hugely between species (Couto et al 2020). Visual information from the eyes is transmitted via photoreceptor axons to the optic lobe, which consists of the lamina, medulla, lobula plate, lobula, accessory medulla, and, in some species, ventral lobula (Strausfeld and Nässel 1980;Kinoshita et al 2015).…”

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confidence: 99%

Neuroanatomical shifts mirror patterns of ecological divergence in three diverse clades of mimetic butterflies

Wainwright

Montgomery

2022

Evolution

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Microhabitat partitioning in heterogenous environmentscan support more diverse communities but may expose partitioned species to distinct perceptual challenges. Divergence across microhabitats could therefore lead to local adaptation to contrasting sensory conditions across small spatial scales, but this aspect of community structuring is rarely explored. Diverse communities of ithomiine butterflies provide an example where closely related species partition tropical forests, where shifts in mimetic coloration are tightly associated with shifts in habitat preference. We test the hypothesis that these mimetic and ecological shifts are associated with distinct patterns of sensory neural investment by comparing brain structure across 164 individuals of 16 species from three ithomiine clades. We find distinct brain morphologies between Oleriina and Hypothyris, which are mimetically homogenous and occupy a single microhabitat. Oleriina, which occurs in low-light microhabitats, invests less in visual brain regions than Hypothyris, with one notable exception, Hyposcada anchiala, the only Oleriina sampled to have converged on mimicry rings found in Hypothyris.We also find that Napeogenes, which has diversified into a range of mimicry rings, shows intermediate patterns of sensory investment. We identify flight height as a critical factor shaping neuroanatomical diversity, with species that fly higher in the canopy investing more in visual structures. Our work suggests that the sensory ecology of species may be impacted by, and interact with, the ways in which communities of closely related organisms are adaptively assembled.

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“…Butterflies are becoming a popular system in the fields of evolutionary neurobiology and neuroethology because they use a large set of sensory modalities for their survival and reproduction [26]. They process visual [27], olfactory [28], auditory [29], and gustatory [30] signals to help them forage, search for a host plant, select mates, avoid predators, or migrate.…”

Section: Introductionmentioning

confidence: 99%

Dissections of Larval, Pupal and Adult Butterfly Brains for Immunostaining and Molecular Analysis

Toh

Dion

Monteiro

2021

MPs

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Butterflies possess impressive cognitive abilities, and investigations into the neural mechanisms underlying these abilities are increasingly being conducted. Exploring butterfly neurobiology may require the isolation of larval, pupal, and/or adult brains for further molecular and histological experiments. This procedure has been largely described in the fruit fly, but a detailed description of butterfly brain dissections is still lacking. Here, we provide a detailed written and video protocol for the removal of Bicyclus anynana adult, pupal, and larval brains. This species is gradually becoming a popular model because it uses a large set of sensory modalities, displays plastic and hormonally controlled courtship behaviour, and learns visual mate preference and olfactory preferences that can be passed on to its offspring. The extracted brain can be used for downstream analyses, such as immunostaining, DNA or RNA extraction, and the procedure can be easily adapted to other lepidopteran species and life stages.

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Linking ecological specialisation to adaptations in butterfly brains and sensory systems

Cited by 21 publications

References 49 publications

Re-emergence and diversification of a specialised antennal lobe morphology in ithomiine butterflies

Re-emergence and diversification of a specialised antennal lobe morphology in ithomiine butterflies

Neuroanatomical shifts mirror patterns of ecological divergence in three diverse clades of mimetic butterflies

Dissections of Larval, Pupal and Adult Butterfly Brains for Immunostaining and Molecular Analysis

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