Biology subjects

Auer, T. O.

Publications and source records attributed to Auer, T. O..

12 recordsLinked to original sources

bioRxiv2024

Evolution of taste processing shifts dietary preference

Food choice is an important driver of speciation and invasion of novel ecological niches. However, we know little about the mechanisms leading to changes in dietary preference. Here, we use the three closely-related species Drosophila sechellia, D. simulans and D. melanogaster to study taste circuit and food choice evolution. D. sechellia, a host specialist, feeds exclusively on a single fruit (Morinda citrifolia, noni) - the latter two are generalists living on various substrates. Using quantitative feeding assays, we recapitulate the preference for noni in D. sechellia and detect conserved sweet but altered bitter sensitivity via calcium imaging in peripheral taste neurons. Noni surprisingly activates bitter sensing neurons more strongly in D. sechellia due to a small deletion in one single gustatory receptor. Using volumetric calcium imaging in the ventral brain, we show that instead of peripheral physiology, species-specific processing of noni and sugar signals in sensorimotor circuits recapitulates differences in dietary preference. Our data support that peripheral receptor changes alone cannot explain altered food choice but rather modifications in how sensory information is transformed into feeding motor commands.

neuroscience↗

bioRxiv2024

Olfactory projection neuron rewiring in the brain of an ecological specialist

Animals behaviours can vary greatly between even closely-related species. While changes in the sensory periphery have frequently been linked to species-specific behaviours, very little is known about if and how individual cell types in the central brain evolve. Here, we develop a set of advanced genetic tools to compare homologous neurons in Drosophila sechellia - which specialises on a single fruit - and Drosophila melanogaster. Through systematic morphological analysis of olfactory projection neurons (PNs), we reveal that global anatomy of these second-order neurons is conserved. However, high-resolution, quantitative comparisons identify a striking case of convergent rewiring of PNs in two distinct olfactory pathways critical for D. sechellias host location. Calcium imaging and labelling of pre-synaptic sites in these evolved PNs demonstrate that novel functional connections with third-order partners are formed in D. sechellia. This work demonstrates that peripheral sensory evolution is accompanied by highly-selective wiring changes in the central brain to facilitate ecological specialisation, and paves the way for systematic comparison of other cell types throughout the nervous system.

neuroscience↗

bioRxiv2023

Meteorins regulate the formation of the left-right organizer and the establishment of vertebrate body asymmetry

While the exterior of vertebrate bodies appears bilaterally symmetrical, internal organ positioning and morphology frequently exhibit left-right (L-R) asymmetries. In several vertebrates, including human, mouse, frog and zebrafish, left-right symmetry-breaking during embryonic development is initiated by a ciliated organ called the Node or left-right organizer. Within the Node, a leftward flow of extraembryonic fluid named the Nodal flow mediates the asymmetric expressions of Nodal factors. Although downstream Nodal pathway components leading to the establishment of the embryonic left-right axis are well known, less is known about the development and formation of the embryonic Node itself. Here we reveal a novel role for the Meteorin protein family in the establishment of the left-right axis and in the formation of the Kupffers vesicle, the Node equivalent structure in zebrafish. We show that the genetic inactivation of each or all three members of the zebrafish Meteorin family (metrn, metrn-like a and metrn-like b) leads to defects in properties of the Kupffers vesicle, caused by impaired assembly and migration of the Kupffers vesicle forming dorsal forerunner cells. In addition, we demonstrate that Meteorins genetically interact with integrins ItgaV and Itg{beta}1b regulating the dorsal forerunner cell clustering and that meteorins loss-of-function results in disturbed Nodal factor expression and consequently in randomized or symmetric heart looping and jogging. These results identify a new role for the Meteorin protein family in the left-right asymmetry patterning during embryonic vertebrate development.

developmental biology↗

bioRxiv2023

Sensory neuron population expansion enhances odour tracking through relaxed projection neuron adaptation

The evolutionary expansion of sensory neuron populations detecting important environmental cues is widespread, but functionally enigmatic. We investigated this phenomenon through comparison of homologous neural pathways of Drosophila melanogaster and its close relative Drosophila sechellia, an extreme specialist for Morinda citrifolia noni fruit. D. sechellia has evolved species-specific expansions in select, noni-detecting olfactory sensory neuron (OSN) populations, through multigenic changes. Activation and inhibition of defined proportions of neurons demonstrate that OSN population increases contribute to stronger, more persistent, noni-odor tracking behavior. These sensory neuron expansions result in increased synaptic connections with their projection neuron (PN) partners, which are conserved in number between species. Surprisingly, having more OSNs does not lead to greater odor-evoked PN sensitivity or reliability. Rather, pathways with increased sensory pooling exhibit reduced PN adaptation, likely through weakened lateral inhibition. Our work reveals an unexpected functional impact of sensory neuron expansions to explain ecologically-relevant, species-specific behavior.

neuroscience↗

bioRxiv2023

Evolution of connectivity architecture in the Drosophila mushroom body

Brain evolution has primarily been studied at the macroscopic level by comparing the relative size of homologous brain centers between species. How neuronal circuits change at the cellular level over evolutionary time remains largely unanswered. Here, using a phylogenetically informed framework, we compare the olfactory circuits of three closely related Drosophila species that differ radically in their chemical ecology: the generalists Drosophila melanogaster and Drosophila simulans that feed on fermenting fruit, and Drosophila sechellia that specializes on ripe noni fruit. We examine a central part of the olfactory circuit that has not yet been investigated in these species -- the connections between the projection neurons of the antennal lobe and the Kenyon cells of the mushroom body, an associative brain center -- to identify species-specific connectivity patterns. We found that neurons encoding food odors -- the DC3 neurons in D. melanogaster and D. simulans and the DL2d neurons in D. sechellia -- connect more frequently with Kenyon cells, giving rise to species-specific biases in connectivity. These species-specific differences in connectivity reflect two distinct neuronal phenotypes: in the number of projection neurons or in the number of presynaptic boutons formed by individual projection neurons. Finally, behavioral analyses suggest that such increased connectivity enhances learning performance in an associative task. Our study shows how fine-grained aspects of connectivity architecture in an associative brain center can change during evolution to reflect the chemical ecology of a species.

neuroscience↗

bioRxiv2022

Odor-gated oviposition behavior in an ecological specialist

Colonization of a novel ecological niche can require, or be driven by, evolution of an animals behaviors promoting their reproductive success in the new environment. Little is known about the underlying mechanisms. We have exploited an emerging genetic model for behavioral neuroecology, Drosophila sechellia - a close relative of Drosophila melanogaster that exhibits extreme specialism for Morinda citrifolia noni fruit - to study the evolution and sensory basis of oviposition. D. sechellia produces fewer eggs compared to other drosophilids, but lays these almost exclusively on noni substrates, contrasting with avoidance or indifference of noni by generalist species. Visual, textural and social cues do not explain the species-specificity of this preference. By contrast, loss of olfactory input in D. sechellia, but not D. melanogaster, essentially abolishes egg-laying, suggesting that this sensory modality gates gustatory-driven noni preference. We find the noni bouquet is detected by redundant olfactory pathways. By parsing the fruits volatile chemicals and genetic perturbation of individual olfactory pathways in D. sechellia, we discover a key role for hexanoic acid and its cognate receptor, the Ionotropic receptor Ir75b, in odor-evoked oviposition. Through receptor exchange in D. melanogaster, we provide evidence for a causal contribution of odor-tuning changes in Ir75b to the evolution of oviposition behavior during D. sechellias host specialization.

animal behavior and cognition↗

bioRxiv2021

Odorant receptor copy number change, co-expression, and positive selection establish peripheral coding differences between fly species

1.Despite numerous examples of chemoreceptor gene family expansions and contractions, how these changes relate to modifications in the neural circuitry in which they are expressed remains unclear. Drosophilas Odorant receptor (Or) family is ideal for addressing this question because a large majority of Ors are uniquely expressed in single olfactory sensory neuron (OSN) types. Between-species changes in Or copy number, therefore, may indicate diversification/reduction of OSN populations. To test this, we investigated a rapidly duplicated/deleted subfamily (named Or67a) in Drosophila melanogaster and its sister species (D. simulans, D. sechellia, and D. mauritiana). We found that the common ancestor had three Or67a paralogs that had already diverged adaptively in their odor-evoked responses. Following their speciation, two Or67a paralogs were lost independently in D. melanogaster and D. sechellia, with ongoing positive selection acting on the intact genes. Instead of the expected singular expression of each diverged Ors, the three D. simulans Or67a paralogs are co-expressed. Thus, while neuroanatomy is conserved between these species, independent selection on co-expressed receptors has contributed to species-specific peripheral coding of olfactory information. This work reveals a model of adaptive change previously not considered for olfactory evolution and raises the possibility that similar processes may be operating among the largely uninvestigated cases of Or co-expression.

evolutionary biology↗

bioRxiv2021

Olfactory receptor-dependent receptor repression in Drosophila

In olfactory systems across phyla, most sensory neurons transcribe a single olfactory receptor gene selected from a large genomic repertoire. We describe novel receptor gene-dependent mechanisms that ensure singular expression of receptors encoded by a tandem gene array in Drosophila. Transcription from upstream genes in the cluster runs through the coding region of downstream loci to inhibit their expression in cis, via transcriptional interference. Moreover, one receptor blocks expression of other receptor proteins in trans through a post-transcriptional mechanism. These repression mechanisms operate in endogenous neurons to ensure their unique expression. Our data provide evidence for inter-olfactory receptor regulation in invertebrates, and highlight unprecedented, but potentially widespread, mechanisms for ensuring exclusive expression of chemosensory receptors, and other protein families, encoded by tandemly-arranged genes.

neuroscience↗

bioRxiv2019

Mate discrimination among subspecies through a conserved olfactory pathway

Signaling mechanisms underlying the sexual isolation of species are poorly understood. Using four subspecies of Drosophila mojavensis as a model, we identify two behaviorally active male-specific pheromones. One functions as a conserved male anti-aphrodisiac in all subspecies and acts via gustation. The second induces female receptivity via olfaction exclusively in the two subspecies that produce it. Genetic analysis of the cognate receptor for the olfactory pheromone indicates an important role for this sensory pathway in promoting sexual isolation of subspecies, in collaboration with auditory signals. Surprisingly, the peripheral sensory pathway detecting this pheromone is conserved molecularly, physiologically and anatomically across subspecies. These observations imply that subspecies-specific behaviors arise from differential interpretation of the same peripheral cue, reminiscent of sexually conserved detection but dimorphic interpretation of male pheromones in D. melanogaster. Our results reveal that, during incipient speciation, pheromone production, detection and interpretation do not necessarily evolve in a coordinate manner.

neuroscience↗

bioRxiv2019

The making of an olfactory specialist

The evolution of animal behaviour is poorly understood. Despite numerous correlations of behavioural and nervous system divergence, demonstration of the genetic basis of interspecific behavioural differences remains rare. Here we develop a novel neurogenetic model, Drosophila sechellia, a close cousin of D. melanogaster that displays profound behavioural changes linked to its extreme host fruit specialisation. Through calcium imaging, we identify olfactory pathways detecting host volatiles. Mutational analysis indicates roles for individual receptors in long- and short-range attraction. Cross-species allele transfer demonstrates that differential tuning of one receptor is important for species-specific behaviour. We identify the molecular determinants of this functional change, and characterise their behavioural significance and evolutionary origin. Circuit tracing reveals that receptor adaptations are accompanied by increased sensory pooling onto interneurons and novel central projection patterns. This work links molecular and neuronal changes to behavioural divergence and defines a powerful model for investigating nervous system evolution and speciation.

neuroscience↗

bioRxiv2018

An expression atlas of chemosensory ionotropic glutamate receptors identifies a molecular basis of carbonation detection

Taste perception is thought to involve the encoding of appetitive and aversive chemical cues in food through a limited number of sensory pathways. Through expression analysis of the complete repertoire of Drosophila Ionotropic Receptors (IRs), a sensory subfamily of ionotropic glutamate receptors, we reveal that the majority of IRs is expressed in diverse peripheral neuron populations across gustatory organs in both larvae and adults, implying numerous roles in taste-evoked behaviours. We characterise Ir56d, which labels two anatomically-distinct classes of neurons in the proboscis: one represents a subset of sugar- and fatty acid-sensing neurons, while the other responds to carbonated solutions and fatty acids. Mutational analysis shows that IR56d, together with the broadly-expressed co-receptors IR25a and IR76b, is essential for physiological activation by carbonation and fatty acids, but not sucrose. We further demonstrate that carbonation is behaviourally attractive to flies (in an IR56d-dependent manner), but in a distinct way to other appetitive stimuli. Our work provides a valuable toolkit for investigating the taste functions of IRs, defines a molecular basis of carbonation sensing, and illustrates how the gustatory system uses combinatorial expression of sensory receptors in distinct neuron types to coordinate behaviour.

neuroscience↗

bioRxiv2016

Second Generation Drosophila Chemical Tags: Sensitivity, Versatility and Speed

Labeling and visualizing cells and sub-cellular structures within thick tissues, whole organs and even intact animals is key to studying biological processes. This is particularly true for studies of neural circuits where neurons form sub-micron synapses but have arbors that may span millimeters in length. Traditionally labeling is achieved by immunofluorescence; however diffusion of antibody molecules (>100 kDa) is slow and often results in uneven labeling with very poor penetration into the centre of thick specimens; these limitations can be partially addressed by extending staining protocols to over a week (Drosophila brain) and months (mice). Recently we developed an alternative approach using genetically encoded chemical tags CLIP, SNAP, Halo and TMP for tissue labeling; this resulted in >100 fold increase in labeling speed in both mice and Drosophila, at the expense of a considerable drop in absolute sensitivity when compared to optimized immunofluorescence staining. We now present a second generation of UAS and LexA responsive CLIP, SNAPf and Halo chemical labeling reagents for flies. These multimerized tags with translational enhancers display up to 64 fold increase in sensitivity over first generation reagents. In addition we developed a suite of conditional reporters (4xSNAPf tag and CLIP-SNAP-Halo) that are activated by the DNA recombinase Bxb1. Our new reporters can be used with weak and strong GAL4 and LexA drivers and enable stochastic, intersectional and multicolor Brainbow labeling. These improvements in sensitivity and experimental versatility, while still retaining the substantial speed advantage that is a signature of chemical labeling, should significantly increase the scope of this technology.

neuroscience↗