The eye is an exquisite anatomical structure and fertile ground for demonstrating core concepts in physics (optics) and biology (evolution by natural selection), a pattern that began with Darwin himself. He described eyes as “organ[s] of extreme perfection and complication” (Darwin 1859, p. 186) and he used them as foil for opposition in one of his most-quoted sentences:
To suppose that the eye with all its inimitable contrivances for adjusting the focus to different distances, for admitting different amounts of light, and for the correction of spherical and chromatic aberration, could have been formed by natural selection, seems, I freely confess, absurd in the highest degree.
Despite his ‘confession,’ Darwin never doubted the evolution of complex eyes, a view that has since received overwhelming support (Lamb et al. 2007; Gregory 2008). At the same time, the eyes and visual systems of animals are wonderfully diverse, a fact that fuels the pages of biology textbooks and fires our natural curiosity. Cronin et al. (2014) put it this way: “We humans are visual creatures. We are also introspective and curious, a combination that makes us all by nature amateur visual ecologists (even if we don’t know it). Because our world is dominated by visual sensations, we naturally wonder how other animals see their particular worlds.” On a philosophical level, we can never know the visual world of another organism (Nagel 1974), but the emergence and spread of immersive technologies enables us to try in the service of constructivist pedagogies (Colburn 2000), as a “way of seeing” fundamental concepts in optics and evolution (Scott et al. 1991).
3D virtual reality learning environments (VRLEs)
Three-dimensional (3D) virtual reality learning environments (VRLEs) are well suited to constructivism, especially when students must form 3D representations of course material or interact with a learning environment to construct knowledge (reviews: Huang et al. 2010; Merchant et al. 2014). Accordingly, the development and deployment of 3D VRLEs has expanded rapidly in K-12 and higher education, especially medical education (Wu et al. 2013; Jang et al. 2017); indeed, the anatomical education of medical students is a major catalyst for 3D VRLE technology. The practical value of 3D VRLEs for learning human anatomy hints at wider applications within K-12 biological education. For example, the principles of natural selection and evolution is another topic that invites constructivist pedagogies (Kalinowski et al. 2013; Lee et al. 2017; Prins et al. 2017). Here we describe a 3D VRLE with this goal in mind. It is intended to demonstrate the principles of visual optics and natural selection in a way that constructs knowledge and stimulates user reflection on diverse worldviews. The inspiration for our 3D VRLE is the tarsier, a primate with an extreme visual system.
Tarsiers and their visual world
Tarsiers are small (113–142 g) nocturnal primates (Fig. 1a). They are an enduring source of fascination for having enormous eyes, both in absolute size and in proportion to the size of the animal (Fig. 1b). Polyak (1957) concluded that the eye size relative to body size of tarsiers is unmatched by any living vertebrate. The extreme eye size of tarsiers is most likely related to the absence of a tapetum lucidum, the mirror-like structure that results in ‘eye shine’ (Cartmill 1980).
A tapetum lucidum is prevalent among nocturnal mammals, including nocturnal primates, because it increases photon capture and visual sensitivity under low light levels. The absence of a tapetum lucidum in tarsiers is therefore puzzling, and it is interpreted as evidence of an ancestral shift from nocturnality to diurnality followed by a reversion to nocturnality with a diurnally-adapted, tapetum-free eye (Cartmill 1980; Martin and Ross 2005). Thus, the hyper-enlarged eyes of tarsiers are widely viewed as a compensatory adaptation to improve visual sensitivity at night in the absence of a tapetum lucidum.
To appreciate why enlarged eyes are advantageous at night, we can use the dimensions of tarsier eyes to calculate the corresponding parameters for humans. For example, the eye-to-brain volume ratio of tarsiers (see Fig. 1b) can be scaled to human dimensions (see Appendix for calculations), to produce an eye with a diameter of 13.6 cm, the approximate volume of a grapefruit (Fig. 2a). The biological plausibility of this thought experiment is attested by the eyes of colossal squid (Mesonychoteuthis hamiltoni), which are nearly twice as large (Nilsson et al. 2012). Yet, the optic axes of these hypothetical eyes would never align with the visual axes of human binocular vision, so we merged the eyes to bring the optic and visual axes into alignment (Fig. 2b). In theory, such tarsier-inspired eyewear would enhance the visual sensitivity of human users (Fig. 2c), as the enlarged corneas would capture more photons under low light levels.
Physical eyewear could demonstrate these principles, but virtual “lenses” enable the use of filters and interactive elements, essentially transcending physical limitations to create specialized environments for intentional exploration. Such a VRLE is exciting because it can better convey visual sensitivity at night by simulating the benefits of having high densities of rod photoreceptors—tarsiers have > 300,000/mm2, whereas humans have ~ 176,000/mm2 (Collins et al. 2005). It can also simulate other aspects of tarsier vision. For example, the visual acuity of Philippine tarsiers is estimated at 8.89 c/deg (Veilleux and Christopher 2009), a minimum resolvable angle that can be simulated for human users (Caves and Johnsen 2017). Another distinguishing trait of tarsiers is red-green colorblindness. This trait varies among species, but each phenotype can be simulated (Melin et al. 2013a, b; Moritz et al. 2017). Lastly, a VRLE can simulate the visual field of tarsiers (186°), which we calculated by summing the visual angle of each eye (156.5°; Fig. 1c) and subtracting the area of binocular overlap (127°; Ross 2000).
Collectively, these traits of the tarsier visual system are predicted to result in superior vision (relative to humans) at night, and they are widely interpreted as adaptations for visual predation—tarsiers are exceptional among primates for being 100% faunivorous (Ross 2004; Moritz et al. 2014, 2017). For humans to appreciate the optical and selective advantages of tarsier eyes for accomplishing this visual challenge (navigation and predation in the dark), we conceived and developed a VRLE in the service of education, science communication, and existential reflection. The result—which we call Tarsier Goggles—can simulate human and tarsier vision under varying ambient lighting conditions.