Dr%20Lauren%20Sumner-Rooney: List of publications

Spatial vision was recently reported in a brittle star, Ophiomastix wendtii, which lacks discrete eyes, but little is known about its visual ecology. Our aim was to better characterize the vision and visual ecology of this unusual visual system. We tested animals’ orientation relative to vertical bar stimuli at a range of angular widths and contrast, to identify limits of angular and contrast detection. We also presented dynamic shadow stimuli, either looming towards or passing overhead the animal, to test for potential defensive responses. Finally, we presented animals lacking a single arm with a vertical bar stimulus known to elicit a response in intact animals. We found that O. wendtii orients to large (≥50°), high-contrast vertical bar stimuli, consistent with a shelter-seeking role and with photoreceptor acceptance angles estimated from morphology. We calculate poor optical sensitivity for individual photoreceptors, and predict dramatic oversampling for photoreceptor arrays. We also report responses to dark stimuli moving against a bright background - this is the first report of responses to moving stimuli in brittle stars and suggests additional defensive uses for vision in echinoderms. Finally, we found that animals missing a single arm orient worse to static stimuli, which requires further investigation.

<jats:title>Abstract</jats:title><jats:p>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 <jats:italic>Parasteatoda tepidariorum</jats:italic> and the harvestman <jats:italic>Phalangium opilio</jats:italic>. 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 <jats:italic>Sox21b-1</jats:italic> likely regulated segmentation ancestrally in arachnids, playing a similar role to the closely related SoxB gene, <jats:italic>Dichaete</jats:italic>, in insects. We previously showed that <jats:italic>Sox21b-1</jats:italic> is required for the simultaneous formation of prosomal segments and sequential addition of opisthosomal segments in <jats:italic>P. tepidariorum</jats:italic>. We studied the expression and function of <jats:italic>Sox21b-1</jats:italic> 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.</jats:p>

Almost all animals can sense light, but only those with spatial vision can ‘see’. Conventionally this was restricted to animals possessing discrete visual organs (eyes), but extraocular vision could facilitate vision without eyes. Echinoderms form the focus of extraocular vision research [1–7], and the brittle star Ophiocoma wendtii, which exhibits light-responsive colour-change and shelter-seeking, became a key species of interest [4,8,9]. Both O. wendtii and an apparently light-indifferent congeneric, O. pumila, possess an extensive network of r-opsin-reactive cells, but its function remains unclear [4]. We show that although both species are strongly light-averse, O. wendtii orients to stimuli necessitating spatial vision for detection, but O. pumila does not. However, O. wendtii’s response disappears when chromatophores are contracted within the skeleton. Combining immunohistochemistry, histology and synchrotron microtomography, we reconstructed models of photoreceptors in situ and extracted estimated angular apertures for O. wendtii and O. pumila. Angular sensitivity estimates, derived from these models, support the hypothesis that chromatophores constitute a screening mechanism in O. wendtii, providing sufficient resolving power to detect the stimuli. RNA-Seq identified opsin candidates in both species, including multiple r-opsins and transduction pathway constituents, congruent with immunohistochemistry and studies of other echinoderms [10,11]. Finally, we note that differing body postures between the two species during experiments may reflect aspect of signal integration. This represents one of the most detailed mechanisms for extraocular vision yet proposed, and draws interesting parallels with the only other confirmed extraocular visual system, that of some sea urchins, which also possess chromatophores.

Light is a fundamentally important biological cue used by almost every animal on earth, to maintain daily rhythms, navigate, forage, find mates or avoid predators. But an enormous number of species live in darkness: in subterranean caves, deep oceans, underground burrows, and within parasitic host bodies, and the loss of eyes appears consistently across these ecosystems. However, the evolutionary mechanisms that lead to the reduction of the visual system remain the subject of great interest and debate more than 150 years after Darwin tackled the issue. Studies of model taxa have discovered significant roles for natural selection, neutral evolution and pleiotropy, but the interplay between them remains unclear. To nail down unifying concepts surrounding the evolution of eye loss, we must embrace the enormous range of affected animals and habitats. The fine developmental details of model systems such as the Mexican cave tetra Astyanax mexicanus have transformed and enriched the field, but these should be complemented by wider studies to identify truly overarching patterns that apply throughout animals. Here, the major evolutionary drivers are placed within a conceptual cost-benefit framework that incorporates the fundamental constraints and forces that influence evolution in the dark. Major physiological, ecological and environmental factors are considered within the context of this framework, which appears faithful to observed patterns in deep-sea and cavernicolous animals. To test evolutionary hypotheses, a comparative phylogenetic approach is recommended, with the goal of studying large groups exhibiting repeated reduction, and then comparing these across habitats, taxa, and lifestyles. Currently, developmental and physiological methods cannot feasibly be used on such large scales, but penetrative imaging techniques could provide detailed morphological data non-invasively and economically for large numbers of species. Comprehensive structural datasets can then be contextualised phylogenetically to examine recurrent trends and associations, and to reconstruct character histories through multiple independent transitions into darkness. By assessing these evolutionary trajectories within an energetic cost-benefit framework, the relationships between fundamental influences can be inferred and compared across different biological and physical parameters. However, substantial numbers of biological and environmental factors affect the evolutionary trajectory of loss, and it is critical that researchers make fair and reasonable comparisons between objectively similar groups.

Photoreception and vision are fundamental aspects of animal sensory biology and ecology, but important gaps remain in our understanding of these processes in many species. The colour-changing brittle star Ophiocoma wendtii is iconic in vision research, speculatively possessing a unique whole-body visual system that incorporates information from nerve bundles underlying thousands of crystalline ‘microlenses’. The hypothesis that these form a sophisticated compound eye-like system regulated by chromatophore movement has been extensively reiterated, with consequent investigations into biomimetic optics and similar ‘visual’ structures in living and fossil taxa. However, no photoreceptors or visual behaviours have ever been identified. We present the first evidence of photoreceptor networks in three Ophiocoma species, both with and without microlenses and colour-changing behaviour. High-resolution microscopy, immunohistochemistry and synchrotron tomography demonstrate that putative photoreceptors cover the animals’ oral, lateral, and aboral surfaces, but are absent at the hypothesised focal points of the microlenses. The structural optics of these crystal ‘lenses’ are an exaptation and do not fulfil any apparent visual role. This contradicts previous studies, yet the photoreceptor network in Ophiocoma appears even more widespread than previously anticipated, both taxonomically and anatomically.

© INVERTEBRATE ZOOLOGY, 2017. All scientific and intellectual endeavours advance by building on earlier observations. In organismal biology, we can in fact directly replicate original studies of morphology and anatomy, when the original material is still present and accessible in the permanent care of museums. We refer to the apparently miraculous “Lazarisation” of these historical specimens, when the application of state-of-the-art scientific techniques brings new life to material in natural history collections. Classical anatomical, histological and palaeontological work established our fundamental understanding of the natural world over centuries of meticulous and dedicated research, much of which remains unsurpassed to this day. Many of these original specimens are still available to active researchers through dedicated permanent collections in the care of universities and museums. An explosion of advancing methods in recent decades has opened new avenues of research that can exploit invaluable historical material. We review the application of novel techniques, primarily new imaging methods, to historic and important specimens. The pursuit of ultra-high resolution magnification, three-dimensional digital modelling, non-invasive scanning techniques, and, increasingly, elemental analyses all have enormous implications for the future of morphology. Palaeontology, comparative anatomy, and development in particular make ideal platforms for the exploitation of these new techniques. These methods are revolutionizing our use of museum collections and reinventing their role in modern morphological research, which comes at a time of increasing threat to collections and museum curation funding. Future innovations in imaging and non-invasive analyses will doubtless accelerate the renewed research efforts dedicated to existing specimens. Most importantly, we celebrate the continued contributions to morphology from these invaluable pieces of our scientific heritage.

Eye reduction occurs in many troglobitic, fossorial, and deep‐sea animals but there is no clear consensus on its evolutionary mechanism. Given the highly conserved and pleiotropic nature of many genes instrumental to eye development, degeneration might be expected to follow consistent evolutionary trajectories in closely related animals. We tested this in a comparative study of ocular anatomy in solariellid snails from deep and shallow marine habitats using morphological, histological, and tomographic techniques, contextualized phylogenetically. Of 67 species studied, 15 lack retinal pigmentation and at least seven have eyes enveloped by surrounding epithelium. Independent instances of reduction follow numerous different morphological trajectories. We estimate eye loss has evolved at least seven times within Solariellidae, in at least three different ways: characters such as pigmentation loss, obstruction of eye aperture, and “lens” degeneration can occur in any order. In one instance, two morphologically distinct reduction pathways appear within a single genus, Bathymophila. Even amongst closely related animals living at similar depths and presumably with similar selective pressures, the processes leading to eye loss have more evolutionary plasticity than previously realized. Although there is selective pressure driving eye reduction, it is clearly not morphologically or developmentally constrained as has been suggested by previous studies.

The position of scaphopods in molluscan phylogeny remains singularly contentious, with several sister relationships supported by morphological and phylogenomic data: Scaphopoda + Bivalvia (Diasoma), Scaphopoda + Cephalopoda (Variopoda), and Scaphopoda + Gastropoda. Nervous system architecture has contributed significant insights to reconstructing phylogeny in the Mollusca and other invertebrate groups, but a modern neurophylogenetic approach has not been applied to molluscs, hampered by a lack of clearly defined homologous characters that can be unequivocally compared across the radical body plan disparity among the living clades. We present the first three-dimensional reconstruction of the anterior nervous system of a scaphopod, Rhabdus rectius, using histological tomography. We also describe a new putative sensory organ, a paired and pigmented sensory mantle slit. This structure is restricted to our study species and not a general feature of scaphopods, but it forms an integral part of the description of the nervous system in R. rectius. It also highlights the potential utility of neuro-anatomical characters for multiple levels of phylogenetic inference beyond this study. This potential has not previously been exploited for the thorny problem of molluscan phylogeny. The neuroanatomy of scaphopods demonstrates a highly derived architecture that shares a number of key characters with the cephalopod nervous system, and supports a Scaphopoda + Cephalopoda grouping.