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Roberts, N. W.

Publications and source records attributed to Roberts, N. W..

5 recordsLinked to original sources

Mutualisms within light microhabitats drive sensory convergence in a mimetic butterfly community

Niche partitioning within variable habitats can expose species to distinct sensory information. Vision is the primary sensory modality used by many animals to interact with their habitat. However, within diurnal terrestrial ecosystems, little is known if, and how, variation in light environments impact species assemblages and visual system evolution. By studying a diverse, sympatric community of mimetic butterflies, we demonstrate that forest architecture creates a mosaic of light microhabitats that drive adaptive sensory convergence and divergence in both peripheral and central sensory systems. Our study provides insights into the dynamic response of visual systems when confronted with similar ecological challenges, and illustrates the wide-reaching consequences of interspecific mutualisms, such as mimicry, on organismal evolution.

evolutionary biology↗

Evolution of Large Eyes in Stromboidea (Gastropoda): Impact of Photic Environment and Life History Traits

AO_SCPLOWBSTRACTC_SCPLOWEyes within the marine gastropod superfamily Stromboidea range widely in size, from 0.2 to 2.3 mm, the latter being the largest known eyes of any gastropod. However, the evolutionary pressures underlying this variation remain unknown. Here, we use the wealth of material available in museum collections to explore the impact of ecological factors that affect light availability (ocean depth, turbidity and diel activity) on the evolution of eye size and structure within Stromboidea. We construct the most taxonomically extensive phylogeny of Stromboidea to date as a framework to investigate these relationships. Our results suggest that depth is a key light-limiting factor in stromboid eye evolution; here, increasing water depth is correlated with increasing aperture width relative to lens diameter (p = 0.043), and therefore an increasing investment in sensitivity in dim light environments. In the clade containing all large-eyed families (Strombidae, Rostellariidae and Seraphsidae), cathemeral species had wider eye apertures relative to lens sizes than diurnal species (p = 0.002), thereby prioritising sensitivity over resolution. These cathemeral species also had smaller body sizes than diurnal species (p = 0.002); this may suggest that animals with smaller shells are more vulnerable to shell-crushing predators, and therefore avoid the higher predation pressure experienced by animals active during the day. Within the large-eyed stromboid clade, ancestral state reconstruction estimates that absolute eye size increased above 1 mm twice independently. Due to the high energetic investment associated with large eye sizes, this repeated increase in eye size suggests that higher performance vision is important in behavioural tasks within these families. In addition, we note that species with more robust escape responses tend to have larger eyes than those that do not: for example, strombids have 1.79 {+/-} 0.31 times the eye size that would be expected from their body size (based on Stromboidea as a whole) and are known to display either a rapid escape response from an approaching predator or withdrawal into the shell. By contrast, the small-eyed xenophorids have 0.59 {+/-} 0.30 times the expected eye size, and are only known to withdraw when threatened.

evolutionary biology↗

Multiple axes of visual system diversity in Ithomiini, an ecologically diverse tribe of mimetic butterflies

The striking structural variation seen in arthropod visual systems can be explained by the overall quantity and spatio-temporal structure of light within habitats coupled with developmental and physiological constraints. However, little is currently known about how fine-scale variation in visual structures arise across shorter evolutionary and ecological scales. In this study, we characterise patterns of interspecific (between species), intraspecific (between sexes) and intraindividual (between eye regions) variation in the visual system of four ithomiine butterfly species. These species are part of a diverse 26-Myr-old Neotropical radiation where changes in mimetic colouration are associated with fine-scale shifts in ecology, such as microhabitat preference. By using a combination of selection analyses on visual opsin sequences, in-vivo ophthalmoscopy, micro-computed tomography (micro-CT), immunohistochemistry, confocal microscopy, and neural tracing, we quantify and describe physiological, anatomical, and molecular traits involved in visual processing. Using these data, we provide evidence of substantial variation within the visual systems of Ithomiini, including: i) relaxed selection on visual opsins, perhaps mediated by habitat preference, ii) interspecific shifts in visual system physiology and anatomy, and iii) extensive sexual dimorphism, including the complete absence of a butterfly-specific optic neuropil in the males of some species. We conclude that considerable visual system variation can exist within diverse insect radiations, hinting at the evolutionary lability of these systems to rapidly develop specialisations to distinct visual ecologies, with selection acting at both the perceptual, processing, and molecular level. Summary statementPhysiological, anatomical, and molecular evidence of extensive visual system variation within a diverse butterfly radiation, hinting at the lability of visual systems to evolve specialisations to distinct visual environments.

evolutionary biology↗

The marine gastropod Conomurex luhuanus (Strombidae) has high-resolution spatial vision and eyes with complex retinas

All species within the conch snail family Strombidae possess large camera-type eyes that are surprisingly well-developed compared to those found in most other gastropods. Although these eyes are known to be structurally complex, very little research on their visual function has been conducted. Here, we use isoluminant expanding visual stimuli to measure the spatial resolution and contrast sensitivity of a strombid, Conomurex luhuanus. Using these stimuli, we show that this species responds to objects as small as 1.06{degrees} in its visual field. We also show that C. luhuanus responds to Michelson contrasts of 0.07, a low contrast sensitivity between object and background. The defensive withdrawal response elicited by visual stimuli of such small angular size and low contrast suggests that conch snails may use spatial vision for the early detection of potential predators. We support these findings with morphological estimations of spatial resolution of 1.04 {+/-} 0.14{degrees}. These anatomical data therefore agree with the behavioural measures and highlight the benefits of integrating morphological and behavioural approaches in animal vision studies. Furthermore, using contemporary imaging techniques including serial block-face scanning electron microscopy (SBF-SEM), in conjunction with transmission electron microscopy (TEM), we found that C. luhuanus have more complex retinas, in terms of cell type diversity, than previous studies of the group have discovered using TEM alone. We found the C. luhuanus retina is comprised of six cell types, including a newly identified ganglion cell and accessory photoreceptor, rather than the previously described four cell types. Summary statementBehavioural trials indicate the eyes of conch snail species Conomurex luhuanus provide high-resolution spatial vision, and morphological examination reveals the retina contains more cell types than those of other gastropods.

ecology↗

Polarization Vision: Overcoming Challenges of Working with a Property of Light We Barely See

In recent years, the study of polarization vision in animals has seen numerous breakthroughs, not just in terms of what is known about the function of this sensory ability, but also in the experimental methods by which polarization can be controlled, presented and measured. Once thought to be limited to only a few animal species, polarization sensitivity is now known to be widespread across many taxonomic groups, and advances in experimental techniques are, in part, responsible for these discoveries. Nevertheless, its study remains challenging, perhaps because of our own poor sensitivity to the polarization of light, but equally as a result of the slow spread of new practices and methodological innovations within the field. In this review, we introduce the most important steps in designing and calibrating polarized stimuli, within the broader context of areas of current research and the applications of new techniques to key questions. Our aim is to provide a constructive guide to help researchers, particularly those with no background in the physics of polarization, to design robust experiments that are free from confounding factors.

animal behavior and cognition↗