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Sondhi, Y.

Publications and source records attributed to Sondhi, Y..

10 recordsLinked to original sources

Convergent evolutionary selection unravels the genetic basis of audition in moths

Hearing in Lepidoptera mediates a range of ecologically important behaviours, including mate communication, predator avoidance, and acoustic signalling. In moths, the evolution of predator-prey interactions with bats has further shaped hearing through a sensory arms race, with repeated co-option of auditory organs to detect and evade echolocating predators. Despite significant prior characterization of the neurophysiology and behaviour of hearing in moths, the genetic basis of hearing is poorly understood in most insects. In this study, we identify a core set of putative auditory genes in Lepidoptera using a combination of homology-based searches from Drosophila and evolutionary rate analyses. We find 56 genes present across all species and investigate whether gene copy number varies among non-hearing and hearing lineages and among 3 different ear types. We discovered seven genes associated with ear type and one with ear presence, but did not find significant losses in gene copy number in non-hearing species. We identified three genes (btv, Dnai2, and nompB) with strong evidence of selection in hearing clades and five genes with weaker evidence of selection. We discuss the potential roles of btv, nompB, and Dnai2 in ciliary transport and the aging of hair cells, as well as the possibility of actively amplified hearing. Our study serves as a primer and resource for further gene mining and functional testing of auditory genes in moths and other insects.

evolutionary biology↗

Superposition eyes of diurnal and nocturnal hawkmoths are imperfect spheres and lack acute zones.

Superposition compound eyes improve sensitivity by pooling light from multiple facets and are widespread among nocturnal insects, including moths and beetles. Optical theory predicts that superposition eyes must be nearly spherical to form coherent images and therefore lack highly pronounced acute zones with high spatial resolution. To examine this, we imaged eyes of six hawkmoths (Sphingidae) spanning diurnal and nocturnal activity with high-resolution microcomputed tomography. Our automated pipeline created detailed eye maps quantifying morphological parameters. We measured local eye curvature (radial distance), interommatidial angle ({Delta}{varphi}), facet size and crystalline cone skewness (tilt of cone axes relative to the local surface normal). All species show more curvature in the dorso-ventral plane with flattening in the antero-posterior plane. However, their eyes still retain near-spherical curvature globally, with diurnal species showing greater distortion. For facet parameters, spatial acuity is generally highest (lowest {Delta}{varphi}) near the eye center and decreases gradually toward the periphery. However, overall variation in spatial acuity is low and these eyes lack distinct acute zones. Facet size gradually changes from center to periphery, increasing in some species and decreasing in the others. Cone skewness is present in all six species (0{degrees}-10{degrees}), but in two diurnal species of hummingbird hawkmoths it increases markedly in the posterior region (15{degrees}-30{degrees}) possibly compensating for regional eye flatness. This paper provides foundational data of ommatidial and eye shape measurements and advances our assumptions about how superposition eyes function.

animal behavior and cognition↗

Gene family evolution reveals dietary adaptations in butterflies and moths

Butterflies and moths (Lepidoptera) are a hyperdiverse lineage of nearly 160,000 described species and their evolutionary success is postulated to be tightly correlated with the radiation of their primary host -- angiosperms. Previous studies found that a significant number of emergent gene families are specific to Lepidoptera, with many genes linked to odorant receptors and peptidases, suggesting that such genetic innovations may be linked to their diversification. Here, we use genomic resources to identify lineage-specific gene families in four nested lepidopteran clades (e.g. Lepidoptera, Glossata, Ditrysia, and Apoditrysia). Among nearly a hundred gene families specific to each group, a handful of gene families have specific and interpretable functions. We found that many digestion-related gene families emerged early in the evolution of Lepidoptera, followed by genes associated with detoxification and immunity. This result aligns with the evolutionary transition in ancient Lepidoptera diets to terrestrial plants, highlighting the emergence of detoxification mechanisms in the megadiverse Ditrysia as a critical adaptation driven by the proliferation of plant chemical defenses. We also found gene families originating from horizontal gene transfer (HGT) events, likely introduced from bacteria and fungi to the common ancestors of Lepidoptera and Ditrysia, respectively. These HGT-derived genes likely played a pivotal role in supporting the dietary transition from algae, diatoms, and aquatic plant debris to fungi and primitive terrestrial plants, ultimately enabling the adaptation to the most dominant angiosperm species.

evolutionary biology↗

Body size and light environment modulate flight speed and saccadic behavior in free flying Drosophila melanogaster

For flying insects, visual control relies on acquiring adequate light, but many circumstances limit this, such as dim environments, high image speeds, or eyes of modest light gathering power. To determine these effects on vinegar flies, we limited light by either placing them in dim conditions, or generating individuals with developmentally smaller eyes, then examined activity levels and three-dimensional flight paths. When simulating dawn and dusk light periods, walking flies increase activity, reflecting their crepuscular nature, and this is stronger for flies with larger eyes. When light switches abruptly, similar to many lab settings, activity associated with crepuscular periods diminishes, as does activity associated with greater facet size. During free flight, we find flight speed decreases similarly in both dim light and small eye conditions, but excess light induces smaller individuals to restore their flight speed. Through a machine learning approach, we confirmed that two features, translational speed and saccade distance, are sufficient to classify treatment groups by light niche, size, and age. Together, these imply that flight changes in smaller individuals result from visual deficits, rather than other elements of body structure.

animal behavior and cognition↗

New genome reveals molecular signatures of adaptation to nocturnality in moth-like butterflies (Hedylidae)

Nearly all animals have a preferred period of daily activity (diel-niche), which is strongly influenced by the light environment. Sensory systems, particularly vision, are adapted to light, and evolutionary transitions to novel light environments, especially light limited ones, can impose strong constraints on eye evolution, color, and motion vision. The adaptive changes in sensory abilities of animals during these transitions, both at the genetic and neural levels, are largely unexplored. Butterflies and moths, with their diverse diel-niche shifts, are an ideal group for investigating the gene evolution linked to these transitions. While most butterflies are day-flying, hedylid butterflies are unique in being primarily nocturnal, and they represent an important evolutionary shift from diurnality to nocturnality in this clade. Here, we sequence the first high-quality Hedylidae genome and functionally annotate genes to understand genomic changes associated with shifts in diel niche. Comparing Hedylidae visual genes against day- and night-flying Lepidoptera species revealed that visual genes are highly conserved, with no major losses. However, hedylid butterfly opsins were more similar to nocturnal moths than their diurnal congeners. Tests on the evolutionary rates (dN/dS) confirmed that color vision opsins were under strong selection, similar to nocturnal moths. We propose that a convergent event of sequence evolution took place when these butterflies became nocturnal, approximately 98 million years ago.

evolutionary biology↗

The developmental gene disco regulates diel-niche evolution in adult moths

AbstractAnimals shift activity periods to reduce predation, minimize competition, or exploit new resources, and this can drive sensory system evolution. But adaptive mechanisms underlying niche- shifts are poorly understood, and model organisms are often too distantly related to reveal the genetic drivers. To address this, we examined expression patterns between two closely related silk moths that have undergone temporal niche divergence. We found 200-700 differentially expressed genes, including day upregulation in eye development and visual processing genes, and night upregulation of antennal and olfactory brain development genes. Further, clusters of circadian, sensory, and brain development genes co-expressed with diel-activity. In both species, eight genes showed expression significantly correlated to diel activity, and are involved in vision, olfaction, brain development, neural plasticity, energy utilization, and cellular maintenance. We repeatedly recovered disco, a zinc- finger transcription factor involved in antennal development, circadian activity, and optic lobe brain development in flies. While disco mutants have circadian arrhythmia, most studies attribute this to improper clock neuron development, not adult circadian maintenance. Comparing predicted 3D protein structure across moth and fly genetic models revealed disco likely retained developmental function with a conserved zinc finger domain, but gained functional zinc finger domains absent in D. melanogaster. These regions have several mutations between nocturnal and diurnal species that co- occur with higher levels of predicted phosphorylation sites. With robust circadian expression, functional nocturnal and diurnal mutations, and structural and sequence conservation, we hypothesize that disco may be a master regulator contributing to diel-activity diversification in adult moths. SignificanceInsect diel-activity patterns are diverse, yet the underlying evolutionary processes are poorly understood. Light environment powerfully entrains circadian rhythms and drives diel-niche and sensory evolution. To investigate its impact, we compared gene expression in closely related day- and night-active wild silk moths, with otherwise similar ecologies. Expression patterns that varied with diel activity included genes linked to eye development, neural plasticity and cellular maintenance. Notably, disco, which encodes a zinc-finger transcription factor involved in pupal Drosophila optic lobe and antennal development, shows robust adult circadian mRNA cycling in moth heads, is highly conserved in moths, and has additional zinc-finger domains with specific nocturnal and diurnal mutations. We hypothesize that disco may contribute to diversification of adult diel-activity patterns in moths.

evolutionary biology↗

Why flying insects gather at artificial light

For millennia, humans have watched nocturnal insects flying erratically around fires and lamps. Explanations have included theories of "lunar navigation" and "escape to light". However, without three-dimensional flight data to test them rigorously, this odd behaviour has remained unexplained. We employed high-resolution motion capture in the laboratory and stereo-videography in the field to reconstruct the 3D kinematics of insect flights around artificial lights. Contrary to the expectation of attraction, insects do not steer directly toward the light. Instead, insects turn their dorsum toward the light, generating flight bouts perpendicular to the source. Under natural sky light, tilting the dorsum towards the brightest visual hemisphere helps maintain proper flight attitude and control. Near artificial sources, however, this highly conserved dorsal-light-response can produce continuous steering around the light and trap an insect. Our guidance model demonstrates that this dorsal tilting is sufficient to create the seemingly erratic flight paths of insects near lights and is the most plausible model for why flying insects gather at artificial lights.

animal behavior and cognition↗

An inexpensive setup for robust activity tracking in small animals: Portable Locomotion Activity Monitor (pLAM)

O_LIAdvances in computer vision and deep learning have automated animal behaviour studies that previously required tedious manual input. However, tracking activity of small and fast flying animals remains a hurdle, especially in a field setting with variable light conditions. Commercial locomotor activity monitors (LAMs) can be expensive, closed source, and generally limited to laboratory settings. C_LIO_LIHere, we present a portable locomotion activity monitor (pLAM), a mobile activity detector to quantify small animal circadian activity. Our setup uses inexpensive components, is based on open-source motion tracking software, and is easy to assemble and use in the field. It runs off-grid, supports low-light tracking with infrared lights, and can implement arbitrary light cycle colours and brightnesses with programmable LEDs. We provide a user-friendly guide to assembling pLAM hardware and accessing its pre-configured software and guidelines for using it in other systems. C_LIO_LIWe benchmarked pLAM for insects under various lab and field conditions, then compared results to a commercial activity detector. They offer broadly similar activity measures, but our setup captures flight and bouts of motion that are often missed by beam-breaking activity detection. C_LIO_LIpLAM will enable high-throughput quantification of small animal location and activity in a low-cost and accessible manner, crucial to studying behaviour that can help inform conservation and management decisions. C_LI

animal behavior and cognition↗

Measuring Compound Eye Optics with Microscope and MicroCT Images

With a great variety of shapes and sizes, compound eye morphologies give insight into visual ecology, development, and evolution, and inspire novel engineering. In contrast to our own camera-type eyes, compound eyes reveal their resolution, sensitivity, and field of view externally, provided they have spherical curvature and orthogonal ommatidia. Non-spherical compound eyes with skewed ommatidia require measuring internal structures, such as with MicroCT (CT). Thus far, there is no efficient tool to characterize compound eye optics, from either 2D or 3D data, automatically. Here we present two open-source programs: (1) the ommatidia detecting algorithm (ODA), which measures ommatidia count and diameter in 2D images, and (2) a CT pipeline (ODA-3D), which calculates anatomical acuity, sensitivity, and field of view across the eye by applying the ODA to 3D data. We validate these algorithms on images, images of replicas, and CT eye scans from ants, fruit flies, moths, and a bee.

neuroscience↗

Light environment drives evolution of color vision genes in butterflies and moths.

Opsins are the primary light-sensing molecules in animals. Opsins have peak sensitivities to specific wavelengths which allows for color discrimination. The opsin protein family has undergone duplications and losses, dynamically expanding and contracting the number of opsins, throughout invertebrate evolution, but it is unclear what drives this diversity. Light availability, however, appears to play a significant role. Dim environments are associated with low opsin diversity in deep-sea fishes and cave-dwelling animals. Correlations between high opsin diversity and bright environments, however, are tenuous. Insects are a good system to test whether opsin expansion is associated with greater light availability because they are enormously diverse and consequently display large variation in diel activity. To test this, we used 200 insect transcriptomes and examined the patterns of opsin diversity associated with diel-niche. We focused on the butterflies and moths (Lepidoptera) because this group has significant variation in diel-niche, substantial opsin recovery (n=100), and particularly well-curated transcriptomes. We identified opsin duplications using ancestral state reconstruction and examined rates of opsin evolution, and compared them across diel-niches. We find Lepidoptera species active in high light environments have independently expanded their opsins at least 10 times. Opsins from diurnal taxa also evolve faster; 13 amino acids were identified across different opsins that were under diversifying selection. Structural models reveal that four of these amino acids overlap with opsin color-tuning regions. By parsing nocturnal and diurnal switches, we show that light environment can influence gene diversity, selection, and protein structure of opsins in Lepidoptera.

evolutionary biology↗