Evidence from the early paleontological record of mammalian evolution has often been interpreted as supporting the idea that mammals were nocturnal for most of their early history. Multiple features of extant mammal sensory systems, such as evolutionary modifications to the light-regulated circadian system, photoreceptor complement, and retinal morphology, support this nocturnal hypothesis for mammalian evolution. Here, we synthesize data on eye shape and orbit orientation in mammals as these data compare to other amniotes. Most mammals differ from other amniotes in retaining an eye design optimized for high visual sensitivity, with the requisite reduction in acuity, which is typically restricted to scotopically (i.e. low light) adapted amniotes. Mammals also possess the more convergent (similarly facing) orbits and, on average, the largest binocular visual fields among amniotes. Based on our analyses, we propose that extant mammals retain a scotopic eye design as well as expanded binocular zones as a result of their nocturnal origin. Only anthropoid primates notably differ from general mammalian patterns, and possibly have evolved an eye shape more typical of the ancestral amniote condition.

Several complementary lines of evidence indicate that mammals originated and evolved within a nocturnal (i.e. low light) environment. For example, many Mesozoic fossil mammals had very small body sizes and insectivorous diets [Kielan-Jaworowska et al., 2004; Luo, 2007]. When compared to extant taxa, the thermoregulatory constraints of small body size and insectivory, among several other factors, suggest that these animals were restricted to the nocturnal environment [Crompton et al., 1978]. Because all extant mammals are ultimately descended from these nocturnal animals, this nocturnal bottleneck had a tremendous influence on the evolution of mammalian sensory system morphology and ecology. Unlike other terrestrial vertebrates, mammals appear to have de-emphasized vision as a distance sense and, instead, have specialized the low-light-friendly distance senses of enhanced olfaction and hearing. Comparatively, mammals have greatly expanded olfactory receptor diversity and have specialized high-frequency hearing [Walls, 1942; Masterson et al., 1969; Jerison, 1973; Frost and Masterson, 1994; reviewed in Streidter, 2005].

Multiple components of the extant mammalian visual apparatus indicate that profound changes occurred during the origin and early evolution of mammals to adapt to a low-light environment. For example, the parietal organ, a photosensitive organ implicated in melatonin synthesis and therefore the regulation of circadian cycles, was lost at the origin of eucynodont therapsids, which are the putative outgroup to mammals [Ali and Klyne, 1985; Hotton et al., 1986; Hopson and Kitching, 2001; Butler and Hodos, 2005]. Although it is not well understood, it appears that the variable loss of parietal foramen and organ in squamates (lizards) tends to be associated with nocturnal, fossorial or otherwise scotopically adapted taxa [Estes et al., 1988; Nydam, pers. comm.]. Mammals also differ from other vertebrates in the complement of Opn4 genes, which encode the extraretinal photopigments. Non-mammalian vertebrates possess both the Opn4x and Opn4m genes that result in expression of extraretinal photopigments found, for instance, in the hypothalamus, pineal organ, lateral septum and retina, to regulate circadian rhythms [Foster and Soni, 1998; Bellingham et al., 2006; Peirson et al., 2009]. Mammals lost the melanopsin encoding Opn4x, and therefore do not express photopigments within brain tissue or other non-retinal structures [Bellingham et al., 2006]. It is hypothesized that the Opn4x in mammals was lost during the long nocturnal period of early mammalian evolution [Foster and Soni, 1998; Bellingham et al., 2006], because the scarce light present under scotopic conditions would be unable to penetrate deep brain tissues sufficiently to activate photopigments for photoentrainment. However, mammals retained melanopsin-containing retinal ganglion cells, which directly communicate with the suprachiasmatic nucleus [Sollars et al., 2003]. Opn4m expression is retained in the retina to mediate rod-cone interactions with ‘on’ and ‘off’ retinal bipolar cells as well as sleep homeostasis [Bellingham et al., 2006; McNeill et al., 2008; Tsai et al., 2009].

It has also been hypothesized that central visual projections in the mammalian brain versus the avian brain reflect the nocturnal bottleneck of mammals. There are two major visual pathways present in all amniote brains, the tectofugal pathway and the thalamofugal pathway. However, in birds the primary visual pathway is the tectofugal, and in mammals it is the thalamofugal. Both pathways begin in the retina, but in the tectofugal pathway the major information relay takes place in the optic tectum (equivalent to the primate superior colliculus); in mammals, less than 5% of retinal efferents take this pathway, which is thought to be involved in encoding gaze direction, at least among anthropoid primates [Sparks, 2004]. In the thalamofugal pathway, the major information relay takes place in the dorsal lateral geniculate nucleus, and nearly all mammalian retinal afferents take this route. In birds the thalamofugal pathway only takes on importance for birds with larger binocular visual fields such as owls, since the lateral geniculate nucleus is the site of the bird secondary partial decussation of fibers, crucial for bringing the visual fields of each eye together to allow for binocular visual integration [Pettigrew, 1978, 1986]. In all non-mammalian amniotes, there is a total decussation of fibers from the right and left eyes at the optic chiasm. In mammals, there is a partial decussation of optic nerve fibers at the optic chiasm, about 10% in the rat and about 50% in primates [Husband and Shimizu, 1999], so a secondary decussation is not necessary. During the nocturnal bottleneck, it may be that mammals both (1) became more dependent on binocular vision as an adaptation for visual sensitivity, resulting in a reorganization of the optic chiasm, and (2) became less dependent on color vision, which was likely originally mediated by the tectofugal pathway [Nguyen et al., 2004]. Both of these factors may have resulted in the increased dependence in mammals on the thalamofugal pathway. Later, when the originally nocturnal mammals began to invade diurnal niches, the thalamofugal pathway may have expanded to include the reduced color vision present in most mammals [Nguyen et al., 2004].

Perhaps most tellingly, however, several features of mammalian eyes themselves appear to indicate a nocturnal ancestry. For example, mammals possess a cone photoreceptor complement reduction from the four found in archosaurs and lepidosaurs to two (fig. 1), with the functional consequence that many mammals are limited to dichromatic color vision [e.g. Jacobs, 1993; Bowmaker, 2008]. Trichromatic mammals, such as some diurnal primates and several metatherians (marsupials), have recently evolved homoplastic cone opsin genes, probably to recapture the chromatic niche occupied by non-mammalian amniotes such as birds that use color cues to detect food items [Jacobs, 1995; Tan and Li, 1999; Heesy and Ross, 2001; Arrese et al., 2002]. The greatly reduced cone complement in conjunction with a substantially rod-dominated retina, again when compared to other amniote taxa, suggests a reduction of visual acuity in favor of light sensitivity in mammals. A de-emphasis on acuity within photopic environments would also potentially explain why eutherian mammals do not possess double cones, which are paired photoreceptors with connecting processes often within the region of the outer plexiform layer of the retina [Djamgoz et al., 1999; Rowe, 2000]. The function of double cones is unclear. However, in many vertebrates, the paired cones often have dissimilar peak wavelength sensitivities (i.e. medium vs. long wavelengths), suggesting that double cones function for color discrimination [Djamgoz et al., 1999]. Additionally, the colored oil droplets typical of many terrestrial tetrapods, which may function to sharpen the tuning of photoreceptors by limiting the range of the spectral responses of the receptor [e.g. Douglas and Marshall, 1999], were lost at the origin of crown-clade mammals. The platypus (Ornithorhynchus anatinus) possesses colorless oil droplets similar to that found in some nocturnal birds, such as owls [Walls, 1942; Ali and Klyne, 1985; Martin, 1985]. Eutherian mammals go one step further and exhibit the complete loss of even colorless oil droplets [Bowmaker et al., 1997; reviewed in Rowe 2000]. Walls [1942] suggested that oil droplet loss is evidence of mammals evolving in a low-light environment because the oil absorbs a significant portion of light, especially at shorter wavelengths [see Rowe, 2000]. Additionally, the accommodation reflex, which alters lens shape in order to focus on objects at variable distances, was lost in monotremes and, variably, in many other mammals. This was also cited by Walls [1942] as an indication of a nocturnal ancestry; the fine focus provided by the accommodation reflex is inherently less useful at night when most vision is blurry anyway [Barrett, 1938; Walls, 1942; Rowe, 2000].

Fig. 1

Distribution of visual traits in mammals and other amniotes. Dashes along internodes indicate possible trait transitions in mammals. Boxes at branch tips indicate the complement of cone opsin genes generally known to be found within each taxon (see text for details). Lepidosaurs are lizards, snakes, and tuataras. Archosaurs are birds and crocodilians. Prototherians, metatherians, and eutherians are monotreme, marsupial, and placental mammals. Key to cone opsin gene families, following Bowmaker [2008]: SWS1 = short wavelength class sensitive in the violet–ultraviolet; SWS2 = short wavelength class sensitive in the blue–violet; RH2 = ‘green’-sensitive with a close homology to rhodopsin; LWS = long wavelength class sensitive in the red–green.

Fig. 1

Distribution of visual traits in mammals and other amniotes. Dashes along internodes indicate possible trait transitions in mammals. Boxes at branch tips indicate the complement of cone opsin genes generally known to be found within each taxon (see text for details). Lepidosaurs are lizards, snakes, and tuataras. Archosaurs are birds and crocodilians. Prototherians, metatherians, and eutherians are monotreme, marsupial, and placental mammals. Key to cone opsin gene families, following Bowmaker [2008]: SWS1 = short wavelength class sensitive in the violet–ultraviolet; SWS2 = short wavelength class sensitive in the blue–violet; RH2 = ‘green’-sensitive with a close homology to rhodopsin; LWS = long wavelength class sensitive in the red–green.

Close modal

When these data are considered in a phylogenetic context, a pattern emerges of changes to the morphology and function of the mammalian visual system relative to other amniotes (fig. 1). Multiple changes implicated in functional specializations to maximum visual sensitivity in low-light environments are concentrated in the last common ancestor of crown clade mammals as well as the last common ancestor of crown clade therian mammals. Taken together, these data support the hypothesis that mammals evolved in a low-light or nocturnal environment.

Although the relationship between all of the aforementioned traits and nocturnality has received considerable attention, the potential for other changes in the visual system coinciding with the ‘nocturnal bottleneck’ of early mammalian evolution has received little treatment. Here, we specifically address how changes in both eye and orbit morphology also support a nocturnal origin of mammals and that the evolutionary changes to the mammalian visual system are far greater than have been previously appreciated.

Activity pattern determines the amount of light available to an animal, and as such is the single most important organizer of the visual apparatus because the optical demands of imaging under plentiful and limited light conditions appear to require different eye shapes [e.g. Land, 1981]. Indeed, comparative studies of eye size and shape in two groups of visually dependent, non-mammalian terrestrial vertebrates, birds [Hall and Ross, 2007; Ross et al., 2007] and lizards [Hall, 2008], both show a robust correlation between eye shape and activity pattern. Nocturnal birds and lizards have larger corneal diameters relative to the axial lengths of the eye, probably to allow more light to enter the eye and thereby increase visual sensitivity. Diurnal birds and lizards, conversely, have a larger axial length of the eye relative to a smaller corneal diameter; an increased axial length allows light to travel further within the eye, increasing the number of photoreceptors over which the image is projected, thereby enhancing visual acuity [Lythgoe, 1979; Land, 1981; Martin, 1982, 1985, 1990; Ross, 2000; Land and Nilsson, 2002; Hall and Ross, 2007; Ross et al., 2007; Hall, 2008].

This robust pattern of eye shape changes in relation to light availability is also observed within anthropoid primates, but it does not extend to non-primate mammals. Instead, non-primates all have a nocturnal eye shape regardless of activity pattern [Ross, 2000; Kirk, 2004, 2006; Ross et al., 2007; Ross and Kirk, 2007]. Behavioral visual acuity data on a variety of birds and mammals verify this pattern. Non-anthropoid mammals, regardless of activity pattern, exhibit visual acuities similar to nocturnal birds, whereas anthropoid primates, including humans, exhibit visual acuities similar to diurnal birds [Ross, 2000; Kirk and Kay, 2004; Harmening et al., 2009] (fig. 2). Kiltie [2000] presented evidence that diurnal mammals overlap with diurnal birds; however, upon inspection his diurnal mammal dataset is comprised entirely of diurnal anthropoid primates. We propose that, in addition to retinal morphology, the loss of oil droplets, and the accommodation reflex, mammalian eye shape is further evidence for the nocturnal bottleneck. Once the mammalian eye had adapted to low-light conditions, that characteristic nocturnal eye shape was maintained in the mammalian radiation, even through the subsequent evolution of diurnality in many lineages. Diurnal owls and diurnal geckos exhibit a similar eye shape pattern in that many retain a nocturnal eye shape with a larger corneal diameter relative to axial length of the eye, even though virtually no other diurnal birds or lizards follow this pattern [Hall and Ross, 2007; Hall, 2008; Hall et al., 2009]. An examination of activity pattern across phylogenies of these two taxa suggests that extant owls and geckos are probably all descended from nocturnal ancestors [Donnellan et al., 1999; Carranza et al., 2002; Wink et al., 2008]. As with mammals, it may be that once owls and geckos evolved a nocturnal eye shape, the subsequent shift of activity pattern did not provide sufficient selection pressure to change eye shape to have a smaller corneal diameter. Martin [1982, 1990] argues strongly that a large corneal diameter does not define a specifically ‘nocturnal’ eye shape. Instead, a large corneal diameter defines an ‘arrhythmic’ eye because regardless of eye shape, in photopic conditions an animal can reduce pupil size through the pupillary reflex without affecting overall eye shape. The same logic may apply to the observed pattern of eye shape in mammals: all but the anthropoid primates maintain a nocturnal eye shape regardless of activity pattern. Interestingly, when mammal and bird eye shapes are plotted together, non-anthropoid mammals occupy the same space as nocturnal birds, and diurnal anthropoids overlap entirely with diurnal birds [Ross et al., 2007; fig. 3]. Thus, the highly visual anthropoids have modified their eye shape, along with the evolution of color vision and higher visual acuity, such that they have converged on birds and lizards and possibly the ancestral condition for vertebrates as a whole.

Fig. 2

The relationship between axial eye diameter (a correlate of focal length) and maximum measured visual acuity in both birds and mammals. Acuity data collected in behavioral studies were used because more of these data are available. Open circles = diurnal mammals; shaded circles = nocturnal mammals; open boxes = diurnal birds; shaded boxes = nocturnal birds; open pentagons = diurnal anthropoid primates; shaded pentagon = nocturnal anthropoid. Visual acuity data are from Kirk and Kay [2004] (for mammals), and Harmening et al., [2009] (for birds). Data on eye sizes are from Ritland [1982] and Hall [2005].

Fig. 2

The relationship between axial eye diameter (a correlate of focal length) and maximum measured visual acuity in both birds and mammals. Acuity data collected in behavioral studies were used because more of these data are available. Open circles = diurnal mammals; shaded circles = nocturnal mammals; open boxes = diurnal birds; shaded boxes = nocturnal birds; open pentagons = diurnal anthropoid primates; shaded pentagon = nocturnal anthropoid. Visual acuity data are from Kirk and Kay [2004] (for mammals), and Harmening et al., [2009] (for birds). Data on eye sizes are from Ritland [1982] and Hall [2005].

Close modal
Fig. 3

Bivariate plots and minimum spanning polygons for axial eye diameter against corneal diameter in birds, non-primate mammals, and anthropoids (monkeys and apes). Black asterisks within nocturnal primate polygon are several diurnal strepsirhine primates. Figure redrawn from Ross et al. [2004].

Fig. 3

Bivariate plots and minimum spanning polygons for axial eye diameter against corneal diameter in birds, non-primate mammals, and anthropoids (monkeys and apes). Black asterisks within nocturnal primate polygon are several diurnal strepsirhine primates. Figure redrawn from Ross et al. [2004].

Close modal

Mammals are notably different from other vertebrates in another aspect of their visual system – orbit orientation and its association with binocular visual field overlap. The position and orientation of the bony orbit within the skull constrains the maximum degree to which the two optic and visual axes can be approximated [Heesy, 2004; see Heesy et al., 2007]. Orbits that are laterally facing prevent overlap between the monocular field of each eye, whereas forward facing orbits allow greater overlap between the monocular fields. Mammals have much higher orbit convergence and binocular visual field overlap than in birds or squamates (i.e. lizards and snakes; fig. 4). The higher orbit convergence values in mammals are related to both quantitative and qualitative differences in binocular visual field overlap when compared to other groups like birds. Interestingly, those birds that are most dependent on binocular vision tend to be nocturnal, and also have a relatively increased dependence on the thalamofugal visual pathway, dominant in binocular-vision-dependent mammals [Husband and Shimizu, 1999]. In mammals, the relationship between orbit convergence and the maximum degree of binocular visual field overlap is virtually isometric [Heesy, 2004] (fig. 5). However, birds display a negative allometric relationship between orbit convergence and maximum degree of binocular visual field overlap [Iwaniuk et al., 2008], although isometry is just included in the confidence intervals. Nevertheless, orbit convergence generally increases more than binocular overlap in interspecific studies of birds (fig. 5). The relationship between orbit convergence and maximum binocular visual field overlap is plotted for both mammals and birds in figure 5. It is notable that although the lower distributions of orbit convergence values are similar between both groups, the distributions of each group overlap minimally. For example, Tyto alba(Common Barn Owl), and Podargus strigoides (Tawny Frogmouth), both nocturnal birds with the highest orbit convergence and maximum binocular visual fields for birds, plot adjacent to Bos taurus (domestic cow) and Mus musculus (mouse) among mammals. The latter two mammals are neither known for their exclusive nocturnal habits nor for expansive binocular zones. Most mammals have more expansive binocular fields – even more than those birds, such as owls, which are notable for their ‘binocular specializations’. These data suggest that mammals and birds may use their binocular visual fields very differently [Martin, 2007, 2009].

Fig. 4

Comparison of orbit convergence in amniotes. Displayed values are for both orbits. Data on mammals are from Heesy [2005]. Data on birds are from Iwaniuk et al. [2008]. Data on snakes and lizards are cadaveric visual field data from Walls [1942]. Cadaveric data on visual fields probably most closely approximate orbit position.

Fig. 4

Comparison of orbit convergence in amniotes. Displayed values are for both orbits. Data on mammals are from Heesy [2005]. Data on birds are from Iwaniuk et al. [2008]. Data on snakes and lizards are cadaveric visual field data from Walls [1942]. Cadaveric data on visual fields probably most closely approximate orbit position.

Close modal
Fig. 5

Relationship between orbit convergence and binocular visual field overlap in mammals and birds. Displayed values are for both orbits. Mammals display an isometric relationship between the two variables (Spearman’s rho = 0.832, p < 0.01; phylogenetic generalized least square correlation r =0.82, p < 0.01; reduced major axis regression slope = 1.2, CI = ± 0.27). Birds display a negatively allometric relationship between the two variables, although the reduced major axis upper confidence interval just includes isometry (Spearman’s rho = 0.81, p < 0.001; reduced major axis regression slope = 0.67, CI = ± 0.34). Open circles = diurnal mammals; shaded circles = nocturnal mammals; open boxes = diurnal birds; shaded boxes = nocturnal birds. Data on mammals are from Heesy [2004], data on birds are from Iwaniuk et al., [2008].

Fig. 5

Relationship between orbit convergence and binocular visual field overlap in mammals and birds. Displayed values are for both orbits. Mammals display an isometric relationship between the two variables (Spearman’s rho = 0.832, p < 0.01; phylogenetic generalized least square correlation r =0.82, p < 0.01; reduced major axis regression slope = 1.2, CI = ± 0.27). Birds display a negatively allometric relationship between the two variables, although the reduced major axis upper confidence interval just includes isometry (Spearman’s rho = 0.81, p < 0.001; reduced major axis regression slope = 0.67, CI = ± 0.34). Open circles = diurnal mammals; shaded circles = nocturnal mammals; open boxes = diurnal birds; shaded boxes = nocturnal birds. Data on mammals are from Heesy [2004], data on birds are from Iwaniuk et al., [2008].

Close modal

The adaptive significance of binocular vision in mammals, especially primates, has variably been related to distance estimation during arboreal locomotion, or to breaking crypsis (camouflage) in nocturnal environments [reviewed in Cartmill, 1992]. Recent analyses of correlated ecological factors with orbit orientation in mammals support the hypothesis that both activity pattern (i.e. available light within the environment) as well as dietary factors explain the most variance in eutherian mammal orbit convergence [Ravosa and Savakova 2004; Heesy, 2004, 2008]. Among non-primate eutherian mammals, nocturnal faunivores (i.e. predators of other animals) have the highest orbit convergence and binocular visual field overlap when compared to other taxa, such as diurnal folivores [Cartmill, 1974, 1992; Ravosa and Savakova, 2004; Heesy, 2004, 2005, 2008, 2009]. These data support the long-held hypothesis that increased binocular overlap confers an adaptive benefit to nocturnal predators, presumably to break camouflage in light-limited environments [e.g. Julesz, 1971; Allman, 1977, 1999; Pettigrew, 1978, 1986; Cartmill, 1992; Heesy, 2008, 2009]. However, the higher orbit convergence values, and by correlation higher binocular visual fields, possessed by mammals in general when compared to birds, lepidosaurs (fig. 4), and possibly most other vertebrates, suggest that mammals may have exploited unique functional properties of binocular vision during their evolutionary history.

Among the functional properties of binocular overlap, parallax for depth judgments, stereopsis (the perception of object solidity in depth), enhanced light sensitivity, and contrast discrimination are the most commonly cited [e.g. Lythgoe, 1979]. Depth perception and stereopsis are reviewed extensively elsewhere [Pettigrew, 1978, 1986; Qian, 1997; DeAngelis, 2000; Heesy, 2009]. Enhanced light sensitivity and contrast discrimination have received less attention, but are likely of equal importance in terms of the evolution of binocularity. Binocular visual fields greatly increase the probability of capturing light within the region of overlap by a factor of approximately 1.25–2 [Pirenne, 1943; Warrant, 2008]. Increasing the probability of light capture is especially beneficial to nocturnal or otherwise scotopically (i.e. vision in low light) adapted taxa. Light levels on a moonless night in a terrestrial environment can be up to 100 million times dimmer than daylight, and there is tremendous variation in light availability from dusk to full night [e.g. Martin, 1990; Warrant, 2004, 2008]. Within aquatic environments, there are examples of mesopelagic fishes (those dwelling 200–900 m underwater) that have evolved dorsally oriented tubular eyes and dorsal binocular overlap to increase visual sensitivity to the region above their heads, from which light is comparatively more abundant [Warrant and Locket, 2004]. Orbit measurements in non-anthropoid primate mammals indicate that nocturnality is correlated consistently with higher orbit convergence values, supporting the idea that nocturnal mammals exploit expanded binocular fields for enhanced light sensitivity (fig. 6). Binocularity also improves contrast discrimination, defined as the ability to detect luminance differences in adjacent objects or multiple parts of the same object. This improved contrast discrimination is made possible by physiological (i.e. cortical) summation of the doubled visual information extracted from the similar images presented to each eye [Pirenne, 1943; Campbell and Green, 1965; see Blake et al., 1981]. Binocular contrast helps distinguish unwanted noise from useful information by physiological summation along the visual pathway. In human psychophysical studies, binocular contrast detection decreases as background contrast increases, suggesting the performance benefit to contrast discrimination within a binocular field is accrued mainly at low contrasts [e.g. Legge, 1981; Moradi and Heeger, 2009]. Although contrast is defined independent of luminance, it is reasonable to suggest that the two benefits to expanded binocular visual fields discussed here – enhanced light sensitivity and contrast discrimination – are complementary effects because increased sensitivity to light lowers the threshold for stimulus detection, especially subtle contrast differences.

Fig. 6

Mammal orbit convergence values in diurnal and nocturnal light environments. Arrythmic taxa (not shown) overlap both distributions. Nocturnal and diurnal taxa are statistically significantly different (Mann Whitney U =2476, p < 0.001; two-sample Kolmogorov-Smirnov Z = 3.13, p < 0.001). Excludes anthropoid primates [see Heesy, 2008]. Data on orbit convergence and activity pattern are from Heesy [2003, 2005].

Fig. 6

Mammal orbit convergence values in diurnal and nocturnal light environments. Arrythmic taxa (not shown) overlap both distributions. Nocturnal and diurnal taxa are statistically significantly different (Mann Whitney U =2476, p < 0.001; two-sample Kolmogorov-Smirnov Z = 3.13, p < 0.001). Excludes anthropoid primates [see Heesy, 2008]. Data on orbit convergence and activity pattern are from Heesy [2003, 2005].

Close modal

Nocturnal eye shape, higher orbit convergence and greater binocular visual field overlap, and a dependence on the thalamofugal visual pathway are derived mammalian traits. Both nocturnal eye shape and binocular overlap confer a light capture advantage within the principal component of the visual field in light-limited environments. It is therefore reasonable to hypothesize that the higher orbit convergence and maximum binocular visual field overlap values possessed by mammals are, like nocturnal eye shapes, the result of a long nocturnal period during early mammalian evolution. The ancestral condition of terrestrial vertebrates as a whole was likely diurnal, and therefore these nocturnal mammals would have evolved from a diurnal ancestor. Whether the suite of traits that we have identified as evidence of the nocturnal bottleneck evolved together or individually is unknown. There are also many unanswered questions in regards to the monotreme (Prototheria) visual system. For example, it is unknown whether or not the Opn4x gene is also lost in monotremes – a question that could be answered quickly by testing these animals for the gene. However, more enigmatically, why do monotremes possess a different short wavelength cone opsin gene than the other mammals? As seen in figure 1, two short wavelength genes are found in terrestrial non-mammals, and for some reason, one of these genes is retained by the monotremes, while the other is retained in the eutherians and metatherians. What are the advantages of one gene or the other? If none, simple character mapping does not explain a likely scenario for how these three groups of mammals would retain different genes. However, regardless of the details of potential evolutionary scenarios, the weight of the different lines of evidence presented here on the mammalian visual system converge on the conclusion that a nocturnal bottleneck in early mammalian history is the most parsimonious explanation for the suite of visual characteristics found in extant mammals today.

We would like to thank Doug Wylie for the generous invitation to participate in the Karger workshop on visual ecology and his patience during the delay in receiving the manuscript. We also thank Doug Wylie and Andrew Iwaniuk for their helpful comments on early drafts of this work. The authors’ research summarized here was supported by the Leakey Foundation (C.P.H.), a grant in aid of reaearch from the Society of Integrative and Comparative Biology, the Frank M. Chapman Memorial Fund, the Field Museum of Natural History Visiting Scholarship, and the Jurassic Foundation (M.I.H.).

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