What is unique about the human eye? Comparative image analysis on the external eye morphology of human and nonhuman great apes

The gaze-signaling hypothesis and the related cooperative-eye hypothesis posit that humans have evolved special external eye morphology, including exposed white sclera (the white of the eye), to enhance the visibility of eye-gaze direction and thereby facilitate conspecific communication through joint-attentional interaction and ostensive communication. However, recent quantitative studies questioned these hypotheses based on new findings that humans are not necessarily unique in certain eye features compared to other great ape species. Therefore, there is currently a heated debate on whether external eye features of humans are distinguished from those of other apes and how such distinguished features contribute to the visibility of eye-gaze direction. This study leveraged updated image analysis techniques to test the uniqueness of human eye features in facial images of great apes. Although many eye features were similar between humans and other species, a key difference was that humans have uniformly white sclera which creates clear visibility of both eye outline and iris; the two essential features contributing to the visibility of eye-gaze direction. We then tested the robustness of the visibility of these features against visual noises such as darkening and distancing and found that both eye features remain detectable in the human eye, while eye outline becomes barely detectable in other species under these visually challenging conditions. Overall, we identified that humans have distinguished external eye morphology among other great apes, which ensures robustness of eye-gaze signal against various visual conditions. Our results support and also critically update the central premises of the gaze-signaling hypothesis.

Experimental evidence for the gaze-signaling hypothesis: White sclera enhances the visibility of eye gaze direction in humans and chimpanzees

Hallmark social activities of humans, such as cooperation and cultural learning, involve eye-gaze signaling through joint attentional interaction and ostensive communication. The gaze-signaling and related cooperative-eye hypotheses posit that humans evolved unique external eye morphology, including exposed white sclera (the white of the eye), to enhance the visibility of eye-gaze for conspecifics. However, experimental evidence is still lacking. This study tested the ability of human and chimpanzee participants to detect the eye-gaze directions of human and chimpanzee images in computerized tasks. We varied the level of brightness and size in the stimulus images to examine the robustness of the eye-gaze directional signal against visually challenging conditions. We found that both humans and chimpanzees detected gaze directions of the human eye better than that of the chimpanzee eye, particularly when eye stimuli were darker and smaller. Also, participants of both species detected gaze direction of the chimpanzee eye better when its color was inverted compared to when its color was normal; namely, when the chimpanzee eye has artificial white sclera. White sclera thus enhances the visibility of eye-gaze direction even across species, particularly in visually challenging conditions. Our findings supported but also critically updated the central premises of the gaze-signaling hypothesis.

On the morphospace of eurypterine sea scorpions

ABSTRACT Eurypterids (sea scorpions) are a group of extinct, marine euchelicerates that have an extensive Palaeozoic record. Despite lacking a biomineralised exoskeleton, eurypterids are abundantly preserved within select deposits. These collections make statistical analyses comparing the morphology of different genera possible. However, eurypterid shape has not yet been documented with modern geometric morphometric tools. Here, we summarise the previous statistical assessments of eurypterid morphology and expand this research by presenting landmark and semi-landmark analyses of 115 eurypterid specimens within the suborder Eurypterina. We illustrate that lateral compound eye morphology and position drives specimen placement in morphospace and separates proposed apex predators from more generalist forms. Additionally, evidence for size clusters in Eurypterus that may reflect ontogeny is uncovered. We highlight the use of geometric morphometric analyses in supporting the naming of new taxa and demonstrate that these shape data represent a novel means of understanding inter-generic ontogenetic trajectories and uncovering developmental changes within the diverse euarthropod group.

Vision-Linked Traits Associated With Antenna Size and Foraging Ecology Across Ants

Visual systems in animals often conspicuously reflect the demands of their ecological interactions. Ants occupy a wide range of terrestrial microhabitats and ecological roles. Additionally, ant eye morphology is highly variable; species range from eyeless subterranean-dwellers to highly visual predators or desert navigators. Through a comparative approach spanning 64 species, we evaluated the relationship between ecology and eye morphology on a wide taxonomic scale. Using worker caste specimens, we developed two- and three-dimensional measurements to quantify eye morphology and position, as well as antennal scape length. Surprisingly, we find limited associations between ecology and most eye traits, however, we recover significant relationships between antennal scape length and some vision-linked attributes. While accounting for shared ancestry, we find that two- and three-dimensional eye area is correlated with foraging niche and ommatidia density is significantly associated with trophic level in our sample of ant taxa. Perhaps signifying a resource investment tradeoff between visual and olfactory or tactile acuity, we find that ommatidia density is negatively correlated with antennal scape length. Additionally, we find that eye position is significantly related to antennal scape length and also report a positive correlation between scape length and eye height, which may be related to the shared developmental origin of these structures. Along with previously known relationships between two-dimensional eye size and ant ecology, our results join reports from other organismal lineages suggesting that morphological traits with intuitive links to ecology may also be shaped by developmental restrictions and energetic trade-offs.

Comparative development and ocular histology between epigean and subterranean salamanders (Eurycea) from central Texas

The salamander clade Eurycea from the karst regions of central Texas provides an ideal platform for comparing divergent nervous and sensory systems since some species exhibit extreme phenotypes thought to be associated with inhabiting a subterranean environment, including highly reduced eyes, while others retain an ancestral ocular phenotype appropriate for life above ground. We describe ocular morphology, comparing three salamander species representing two phenotypes—the surface-dwelling Barton Springs salamander (E. sosorum) and San Marcos salamander (E. nana) and the obligate subterranean Texas blind salamander (E. rathbuni) - in terms of structure and size of their eyes. Eyes were examined using confocal microscopy and measurements were made using ImageJ. Statistical analysis of data was carried out using R. We also provide a developmental series and track eye development and immunolocalization of Pax6 in E. sosorum and E. rathbuni. Adult histology of the surface-dwelling San Marcos salamander (E. nana) shows similarities to E. sosorum. The eyes of adults of the epigean species E. nana and E. sosorum appear fully developed with all the histological features of a fully functional eye. In contrast, the eyes of E. rathbuni adults have fewer layers, lack lenses and other features associated with vision as has been reported previously. However, in early developmental stages eye morphology did not differ significantly between E. rathbuni and E. sosorum. Parallel development is observed between the two phenotypes in terms of morphology; however, Pax6 labeling seems to decrease in the latter stages of development in E.rathbuni. We test for immunolabeling of the visual pigment proteins opsin and rhodopsin and observe immunolocalization around photoreceptor disks in E. nana and E. sosorum, but not in the subterranean E. rathbuni. Our results from examining developing salamanders suggest a combination of underdevelopment and degeneration contribute to the reduced eyes of adult E. rathbuni.

Diversity in Primate External Eye Morphology: Previously Undescribed Traits and Their Potential Adaptive Value

Comparative examinations of external eye morphology in primates initially focused on communicative functions of the eye. Subsequent work has failed to find consistent associations between specific eye morphologies and communicative functions. In this article, we review the field of primate external eye morphology and inspect publicly available and unpublished photographs. We identify and describe five commonly occurring traits that have not received attention so far. We cross-examined the clinical and psychological literature to propose potential adaptive functions. These potential adaptive functions include communicative functions, but also photoregulatory functions and photoprotective functions.

Have the eyes of bioluminescent scale worms adapted to see their own light? A comparative study of eyes and vision in Harmothoe imbricata and Lepidonotus squamatus

Annelids constitute a diverse phylum with more than 19000 species, exhibiting greatly varying morphologies and lifestyles ranging from sessile detritivores to fast swimming active predators. The lifestyle of an animal is closely linked to its sensory systems not least the visual equipment. Interestingly, many errant annelid species from different families such as the scale worms, Polynoidae, share the same two pairs of eyes on their prostomium. These eyes are typically 100-200 µm in diameter and structurally similar judged from the gross morphology. The polynoids, Harmothoe imbricata and Lepidonotus squamatus from the North Atlantic are both benthic predators preying on small invertebrates but only H. imbricata can produce bioluminescence in their scales. Here we have examined their eye morphology, photoreceptor physiology, and light guided behaviour in order to assess their visual capacity and visual ecology. Whereas the structure and physiology of the two pairs of eyes are remarkably similar within species, the only difference being the gaze direction, the photoreceptor physiology differs between the two species. Both species express a single opsin in their eyes but in H. imbricata the peak sensitivity is green shifted and the temporal resolution is lower, suggesting that the eyes of H. imbricata are adapted to detect their own bioluminescence. The behavioural experiments showed that both species are strictly night active but yielded no support to the hypothesis that H. imbricata are repelled by their own bioluminescence.