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Abuin, L.

Publications and source records attributed to Abuin, L..

8 recordsLinked to original sources

Temporal niche partitioning through olfactory cell type evolution

Temporal niche partitioning enables species to use the same resource at different times, but the underlying mechanisms are unknown. We show that Drosophila sechellia, a specialist on Morinda citrifolia noni, exhibits narrow temporal preference for the most toxic, ripe fruit, reducing exposure to competition, parasitization and microbial infection that can occur on other stages. Chemical analysis highlighted ketones as signature odors of ripe noni. Comparative single-cell transcriptomic atlases revealed that D. sechellia has co-opted expression of a larval ketone receptor, Or45a, in an adult olfactory neuron population. The novel expression of Or45a can be ascribed solely to cis-regulatory changes and is sufficient to confer physiological sensitivity to ripe noni. Importantly, Or45a is required for D. sechellia's ripe noni preference, acting redundantly with a second ketone receptor, Or85c/b, whose neuron population has expanded in D. sechellia. Our results provide an unprecedented link between cell type evolution and ecologically-advantageous, temporal niche partitioning.

neuroscience↗

Laboratory and wild Drosophila sechellia have conserved niche specialization phenotypes

A major challenge to investigating the proximate causes of ecological adaptation is the difficulty of studying the phenotypes of organisms in their natural environments. By necessity, many studies seeking to determine the genetic and cellular basis of adaptation therefore investigate potentially adaptive phenotypes under laboratory conditions where organisms are more easily experimentally manipulated. For laboratory models, it remains unclear if organisms maintained long term under laboratory conditions are representative of relatives in their natural environment. In recent years, Drosophila sechellia, a specialist species endemic to the Seychelles, has emerged as a (neuro)genetic model for studying the molecular basis of ecological adaptation. A multitude of studies have investigated the genetic and cellular basis of various aspects of this species specialization in a laboratory setting. However, the vast majority of these studies use laboratory strains of D. sechellia that were collected many decades ago, and have been maintained under conditions very different from their natural niche. Thus, it remains unclear if and how these strains resemble their wild counterparts. Here, we compare the phenotypes of these laboratory strains with recently-collected wild D. sechellia to ask if laboratory strains display a loss or degradation of phenotypes potentially involved in their specialization resulting from their long-term laboratory maintenance. Across several behavioral and anatomical phenotypes, we find a high degree of similarity between wild-caught and laboratory-maintained strains. Our results suggest that studies of the molecular mechanisms underlying D. sechellias phenotypes associated with specialization are likely representative of the evolution of these flies in the wild.

evolutionary biology↗

A GPCR signaling pathway in insect odor detection

Odor detection differs fundamentally in vertebrates, which use G protein-coupled receptors (GPCRs)1,2, and insects, which employ ion channels3,4. Here, we report the first evidence for a GPCR defining tuning properties of insect olfactory sensory neurons. Single-cell transcriptomics of the Drosophila melanogaster antenna identified selective expression of the G{gamma}30A subunit in acid-sensing Ir64a-DC4 neurons5,6. G{gamma}30A is essential for broadening responses to long-chain acids, acting with Gs, G{beta}13F, adenylate cyclase Ac13E and the Cngl channel. We further discovered that Cirl, a latrophilin-family GPCR7, is broadly-transcribed in the antenna but the protein is localized only in Ir64a-DC4 sensory cilia, dependent upon G{gamma}30A, but not Ir64a. Importantly, loss of Cirl also narrows Ir64a-DC4 tuning properties. Homologous neurons in Drosophila sechellia naturally exhibit narrow acid tuning, despite functional conservation of Ir64a; these differences correlate instead with lower expression of metabotropic components. Our findings reveal unexpected roles for GPCR/metabotropic signaling in olfactory detection and divergence in insects.

neuroscience↗

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↗

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↗

Evolution of circadian behavioral plasticity through cis-regulatory divergence of a neuropeptide gene

Widely-distributed species experience substantial environmental variation, which they often accommodate through behavioral plasticity. Although this ability is integral to fitness, we have little understanding of the mechanistic basis by which plasticity evolves. One factor that varies seasonally and by latitude is photoperiod (day length). Many organisms, including the cosmopolitan Drosophila melanogaster display circadian plasticity, adjusting to fluctuating photoperiod by varying the timing of their activity to coincide with changing dawn/dusk intervals1. Here, we compare D. melanogaster with the closely-related ecological specialist Drosophila sechellia, an equatorial island endemic that experiences minimal photoperiod variation, to investigate the molecular-genetic basis of circadian plasticity evolution2,3. We discover that D. sechellia displays exceptionally little circadian plasticity compared to D. melanogaster and other non-equatorial drosophilids. Through a screen of circadian mutants in D. melanogaster/D. sechellia hybrids, we identify a role of the neuropeptide Pigment-dispersing factor (Pdf) in this loss. While the coding sequence of Pdf is conserved, we show that Pdf has undergone cis-regulatory divergence in these drosophilids. We document species-specific temporal dynamic properties of Pdf RNA and protein expression, as well as Pdf neuron morphological plasticity, and demonstrate that modulating Pdf expression in D. melanogaster can influence the degree of behavioral plasticity. Furthermore, we find that the Pdf regulatory region exhibits signals of selection across populations of D. melanogaster from different latitudes. Finally, we provide evidence that plasticity confers a selective advantage for D. melanogaster at higher latitudes, while D. sechellia likely suffers fitness costs through reduced copulation success outside its range. Our work defines Pdf as a locus of evolution for circadian plasticity, which might have contributed to both D. melanogasters global distribution and D. sechellias habitat specialization. Moreover, together with spatial changes in Pdf expression reported in high-latitude drosophilid species4,5, our findings highlight this neuropeptide gene as a hotspot for circadian plasticity evolution.

evolutionary biology↗

In vivo assembly and trafficking of olfactory Ionotropic Receptors

lonotropic Receptors (IRs) are a large, divergent subfamily of ionotropic glutamate receptors(iGluRs), with roles in chemosensation, thermosensation and hygrosensation. Analogous to the synaptic targeting mechanisms of their iGluR ancestors, IRs are thought to form complexes of broadly-expressed co-receptors and selectively-expressed tuning receptors to localise to sensory cilia. While tuning receptors extracellular ligand-binding domain (LBD) defines sensory specificity, the role of this domain in co-receptors is unclear. We identify a coreceptor-specific sequence in the LBD, which contains a single N-glycosylation site. Combining molecular genetic and cell biological analyses, we show that this site is dispensable for assembly of IR complexes in olfactory sensory neurons, but essential for endoplasmic reticulum exit of some,but not all, IR complexes. Our data reveal an important role for the IR co-receptor LBD in control of intracellular transport, provide novel insights into the stoichiometry and assembly of IR complexes, and uncover an unexpected heterogeneity in the trafficking regulation of this sensory receptor family.

neuroscience↗

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↗