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Sumner-Rooney, L.

Publications and source records attributed to Sumner-Rooney, L..

10 recordsLinked to original sources

ctSpyderFields: A Python package for visual field reconstruction in spiders

1The measurement of visual fields in arachnology has a long-standing history. Given the wide variety of eye positions, orientation and structure, the topic is fundamental for studies of taxonomy, evolution, ecology and behavior. The existing methods for measuring visual fields deploy ophthalmoscopic measurements, which require custom microscopes, anatomical structures like the reflective tapetum, which may not always be present, or the capacity to detect photoreceptor autofluorescence. Here we present the ctSpyderFields python package: a tool for geometrically predicting the visual fields of arachnids from digital images of the lens and retina. The tool uses images coming from computed tomography (CT) scans of specimens, but could be applied to other 3D microscopy techniques, to virtually project the boundaries of the retina through the geometrically predicted nodal point of the lens, deriving a rough per-eye visual field both in cartesian and spherical coordinates. The extracted data can then be used to calculate likely visual field overlap between eyes and angular spans, which can be compared within or between species. We also provide a use case, reporting the visual field data extracted from a museum specimen of Philaeus crysops. We propose that the tool will allow a wider comparative analysis of visual fields across spider species, unlocking the potential for a deeper understanding of visual ecology and evolution.

bioinformatics↗

Differential evolutionary and ecological patterns in eye loss between parallel visual systems in spiders

Eye loss has long fascinated evolutionary biologists and occurs across the animal kingdom. Spiders have two parallel visual systems -- two primary and six secondary eyes -- but eye losses, leaving six, four, two, or no eyes, have occurred in multiple lineages. Despite their significance, reports of eye loss are scattered, limiting broader analysis. Here we present the first comprehensive analysis of eye loss across all known spider lineages. We show that eye loss occurs in [~]12% of extant species, mainly within the clade Synspermiata. Six-eyed spiders are most common (>5,300 species), while four-eyed, two-eyed, and eyeless forms are rarer and often linked to troglobitic lifestyles. Principal eye loss is widespread, occurring in 49 families across nearly all major lineages. Using a recent phylogeny of the order Araneae, we demonstrate a strong correlation between eye loss and occupancy of low-light environments, but this is complicated by differential effects across eye types and phylogenetic groups through geological time. These findings reveal striking lability in eye number and lay groundwork for future research into ecological, developmental, and neurological drivers of eye loss. [hidden Markov models, ancestral state reconstruction, Araneae, discrete character evolution, principal eyes, secondary eyes, low light environments].

zoology↗

Pre-cheliceral region patterning in a spider provides new insights into the development and evolution of arthropod neurosecretory centres

Comparing head development among arthropods has helped identify ancestral aspects of brain patterning and structure in these animals and more broadly. Most understanding of arthropod head patterning has been learned from insects and the myriapod Strigamia maritima. Chelicerates represent an outgroup to mandibulate arthropods and can provide a valuable perspective to arthropod evolution and development. We assayed the expression of key markers of head patterning and neurosecretory centres in mandibulates in the pre-cheliceral region of embryos of the spider Parasteatoda tepidariorum. We found that, like mandibulates, this spider likely has a pars intercerebralis, marked by six3.2 and visual system homeobox/chx. We also found some evidence for another neurosecretory centre, the pars lateralis, marked by six3.2 and fasciclin 2. Furthermore, we identified anterior-medial cells in the spider pre-cheliceral region that express six3.2, foxQ2, and collier1, suggesting they may be pioneer neurons. However, these spider cells do not appear to be equivalent to the central pioneer neuronal cells identified in S. maritima because they lack expression of other key markers. Taken together, our study of spider pre-cheliceral region patterning adds a new chelicerate perspective to understanding the development and evolution of the arthropod head.

developmental biology↗

Complex allometric relationships and ecological factors shape the development and evolution of eye size in the modular visual system of spiders

Eye size affects many aspects of visual function, most notably including contrast sensitivity and achievable spatial resolution, but eyes are costly to grow and maintain. The allometry of eyes can provide insight to this trade-off in the context of visual ecology, but to date, this has mainly been explored in species that have a single pair of eyes of equal size. By contrast, animals possessing larger visual systems can exhibit variable eye sizes within individuals. Spiders have up to four pairs of eyes whose size often varies, but their ontogenetic, static, and evolutionary allometry has not yet been studied in a comparative context. We report variable evolutionary and developmental dynamics in eye size across 1098 individuals in 39 species and 8 families, indicating selective pressures and constraints driving the evolution of different eye pairs and lineages. We observed variation in the relationship between eye and body size not only between taxa and visual ecologies, but between eye pairs within species, indicating that growth dynamics are variable and can be divergently adapted in particular eye pairs. Supplementing our sampling with a phylogenetically comprehensive dataset recently published by Wolff et al. (2022), we confirmed these findings across more than 400 species, found that ecological factors such as visual hunting, web building, and diurnality can also impact eye diameter, and identified significant allometric shifts across spider phylogeny using an unbiased approach, many of which coincide with ecological changes such as visual pursuit hunting strategies. This study represents the first detailed comparative exploration of visual allometry in spiders, revealing striking differences in eye growth not only between families but also within species. Our findings shed light on the relationship between spider visual systems and their diverse ecologies, and how spiders exploit the modular nature of their visual systems to balance selective pressures and optical and energetic constraints.

evolutionary biology↗

Development and patterning of a highly versatile visual system in spiders

Visual systems provide a key interface between organisms and their surroundings, and have evolved in many forms to perform diverse functions across the animal kingdom. Spiders exhibit a range of visual abilities and ecologies, the diversity of which is underpinned by a highly versatile, modular visual system architecture. This typically includes eight eyes of two developmentally distinct types, but the number, size, location, and function of the eyes can vary dramatically between lineages. Previous studies of visual system development in spiders have confirmed that many components of the retinal determination gene (RDG) network are conserved with other arthropods, but so far, comparative studies among spiders are lacking. We characterised visual system development in eight species of spiders representing a range of morphologies, visual ecologies, and phylogenetic positions, to determine how these diverse configurations are formed, and how they might evolve. Combining synchrotron radiation tomography, transcriptomics, in situ hybridisation, and selection analyses, we characterise the repertoires and expression of key RDGs in relation to adult morphology. We identify key molecular players, timepoints, and developmental events that may contribute to adult diversity, in particular the molecular and developmental underpinnings of eye size, number, position, and identity across spiders.

developmental biology↗

Evolution of compound eye morphology underlies differences in vision between closely related Drosophila species

Insects have evolved complex visual systems and display an astonishing range of adaptations for diverse ecological niches. Differences in eye size within and between Drosophila species provide the opportunity to study the impact of eye structure on vision. Here we further explored differences in D. mauritiana and its sibling species D. simulans and confirmed that D. mauritiana have rapidly evolved larger eyes as a result of more and wider ommatidia than D. simulans since their recent common ancestor. The functional impact of eye size, and specifically ommatidia size, is often only estimated based on the rigid surface morphology of the compound eye. Therefore, we used 3D synchrotron radiation tomography to measure optical parameters in 3D, predict optical capacity, and compare the modelled vision to in vivo optomotor responses. Our optical models predicted higher contrast sensitivity for D. mauritiana, which we verified by presenting sinusoidal gratings to tethered flies in a flight arena. Similarly, we confirmed the higher spatial acuity predicted for Drosophila simulans with smaller ommatidia and found evidence for higher temporal resolution.

evolutionary biology↗

Evolution of the spider homeobox gene repertoire by tandem and whole genome duplication

Gene duplication generates new genetic material that can contribute to the evolution of gene regulatory networks and phenotypes. Duplicated genes can undergo subfunctionalisation to partition ancestral functions and/or neofunctionalisation to assume a new function. We previously found there had been a whole genome duplication (WGD) in an ancestor of arachnopulmonates, the lineage including spiders and scorpions but excluding other arachnids like mites, ticks, and harvestmen. This WGD was evidenced by many duplicated homeobox genes, including two Hox clusters, in spiders. However, it was unclear which homeobox paralogues originated by WGD versus smaller-scale events such as tandem duplications. Understanding this is key to determining the contribution of the WGD to arachnopulmonate genome evolution. Here we characterised the distribution of duplicated homeobox genes across eight chromosome-level spider genomes. We found that most duplicated homeobox genes in spiders are consistent with an origin by WGD. We also found two copies of conserved homeobox gene clusters, including the Hox, NK, HRO, Irx, and SINE clusters, in all eight species. Consistently, we observed one copy of each cluster was degenerated in terms of gene content and organisation while the other remained more intact. Focussing on the NK cluster, we found evidence for regulatory subfunctionalisation between the duplicated NK genes in the spider Parasteatoda tepidariorum compared to their single-copy orthologues in the harvestman Phalangium opilio. Our study provides new insights into the relative contributions of multiple modes of duplication to the homeobox gene repertoire during the evolution of spiders and the function of NK genes.

evolutionary biology↗

Differences in orthodenticle expression promote ommatidial size variation between Drosophila species

The compound eyes of insects exhibit extensive variation in ommatidia number and size, which affects how they see and underlies adaptations in their vision to different environments and lifestyles. However, very little is known about the genetic and developmental bases of differences in compound eye size. We previously showed that the larger eyes of Drosophila mauritiana compared to D. simulans is generally caused by differences in ommatidia size rather than number. Furthermore, we identified an X-linked chromosomal region in D. mauritiana that results in larger eyes when introgressed into D. simulans. Here, we used a combination of fine-scale mapping and gene expression analysis to further investigate positional candidate genes on the X chromosome. We found earlier expression of orthodenticle (otd) during ommatidial maturation in third instar larvae in D. mauritiana than in D. simulans, and we show that this gene is required for the correct organisation and size of ommatidia in D. melanogaster. We discovered that the activity of an otd eye enhancer is consistent with the difference in the expression of this gene between species, with the D. mauritiana enhancer sequence driving earlier expression than that of D. simulans. We also identified potential direct targets of Otd that are differentially expressed between D. mauritiana and D. simulans during ommatidial maturation. Taken together, our results suggest that differential timing of otd expression contributes to natural variation in ommatidia size between D. mauritiana and D. simulans, which provides new insights into the mechanisms underlying the regulation and evolution of compound eye size in insects.

evolutionary biology↗

The evolution of Sox gene repertoires and regulation of segmentation in arachnids

The Sox family of transcription factors regulate many processes during metazoan development, including stem cell maintenance and nervous system specification. Characterising the repertoires and roles of these genes can therefore provide important insights into animal evolution and development. We further characterised the Sox repertoires of several arachnid species with and without an ancestral whole genome duplication (WGD), and compared their expression between the spider Parasteatoda tepidariorum and the harvestman Phalangium opilio. We also found that most Sox families have been retained as ohnologs after WGD and evidence for potential subfunctionalisation and/or neofunctionalization events. Our results also suggest that Sox21b-1 likely regulated segmentation ancestrally in arachnids, playing a similar role to the closely related SoxB gene, Dichaete, in insects. We previously showed that Sox21b-1 is required for the simultaneous formation of prosomal segments and sequential addition of opisthosomal segments in P. tepidariorum. We studied the expression and function of Sox21b-1 further in this spider and found that while this gene regulates the generation of both prosomal and opisthosomal segments, it plays different roles in the formation of these tagmata reflecting their contrasting modes of segmentation and deployment of gene regulatory networks with different architectures.

developmental biology↗

Characterisation of the genetic architecture underlying eye size variation within Drosophila melanogaster and Drosophila simulans

The compound eyes of insects exhibit striking variation in size, reflecting adaptation to different lifestyles and habitats. However, the genetic and developmental bases of variation in insect eye size is poorly understood, which limits our understanding of how these important morphological differences evolve. To address this, we further explored natural variation in eye size within and between four species of the Drosophila melanogaster species subgroup. We found extensive variation in eye size among these species, and flies with larger eyes generally had a shorter inter-ocular distance and vice versa. We then carried out quantitative trait loci (QTL) mapping of intra-specific variation in eye size and inter-ocular distance in both D. melanogaster and D. simulans. This revealed that different genomic regions underlie variation in eye size and inter-ocular distance in both species, which we corroborated by introgression mapping in D. simulans. This suggests that although there is a trade-off between eye size and inter-ocular distance, variation in these two traits is likely to be caused by different genes and so can be genetically decoupled. Finally, although we detected QTL for intra-specific variation in eye size at similar positions in D. melanogaster and D. simulans, we observed differences in eye fate commitment between strains of these two species. This indicates that different developmental mechanisms and therefore, most likely, different genes contribute to eye size variation in these species. Taken together with the results of previous studies, our findings suggest that the gene regulatory network that specifies eye size has evolved at multiple genetic nodes to give rise to natural variation in this trait within and among species.

evolutionary biology↗