Adaptive genomic evolution of opsins reveals that early mammals flourished in nocturnal environments.

BACKGROUND: Based on evolutionary patterns of the vertebrate eye, Walls (1942) hypothesized that early placental mammals evolved primarily in nocturnal habitats. However, not only Eutheria, but all mammals show photic characteristics (i.e. dichromatic vision, rod-dominated retina) suggestive of a scotopic eye design. RESULTS: Here, we used integrative comparative genomic and phylogenetic methodologies employing the photoreceptive opsin gene family in 154 mammals to test the likelihood of a nocturnal period in the emergence of all mammals. We showed that mammals possess genomic patterns concordant with a nocturnal ancestry. The loss of the RH2, VA, PARA, PARIE and OPN4x opsins in all mammals led us to advance a probable and most-parsimonious hypothesis of a global nocturnal bottleneck that explains the loss of these genes in the emerging lineage (> > 215.5 million years ago). In addition, ancestral character reconstruction analyses provided strong evidence that ancestral mammals possessed a nocturnal lifestyle, ultra-violet-sensitive vision, low visual acuity and low orbit convergence (i.e. panoramic vision). CONCLUSIONS: Overall, this study provides insight into the evolutionary history of the mammalian eye while discussing important ecological aspects of the photic paleo-environments ancestral mammals have occupied.

Did trichromatic color vision and red hair color coevolve in primates?

Reddish pelage and red hair ornaments have evolved many times, independently, during primate evolution. It is generally assumed that these red-coat phenotypes, like red skin phenotypes, play a role in sociosexual signaling and, thus evolved in tandem with conspecific color vision. This study examines the phylogenetic distribution of color vision and pelage coloration across the primate order to ask: (1) did red pelage and trichromacy coevolve; or (2) did trichromacy evolve first, and then subsequently red pelage evolved as an exaptation? We collected quantitative, color-corrected photographic color data for 142 museum research skins from 92 species representing 41 genera spanning all major primate lineages. For each species, we quantified the ratio of Red/Green values (from a RGB color model) at 20 anatomical landmarks. For these same species, we compiled data on color vision type (routine trichromatic, polymorphic, routine dichromatic, monochromatic) and data on variables that potentially covary with visual system (VS) and coloration, including activity pattern and body mass dimorphism (proxy for sexual selection). We also considered whether the long-term storage of research skins might influence coloration. Therefore, we included the time since the specimen was collected as an additional predictor. Analyzing the data with phylogenetic generalized least squares models, we found that the amount of red hair present in primates is associated with differences in VSs, but not in the direction expected. Surprisingly, trichromatic primate species generally exhibited less red hair compared to red-green colorblind species. Thus, our results do not support the general assumption that color vision and red pelage coloration are a coevolutionary product of sociosexual signaling in primates. In addition, we did not find an effect of activity pattern, body mass dimorphism, or time since collection on the redness of primate hair. Our results have important implications for the evolution of primate coloration and visual systems.

A novel method for comparative analysis of retinal specialization traits from topographic maps.

Vertebrates possess different types of retinal specializations that vary in number, size, shape, and position in the retina. This diversity in retinal configuration has been revealed through topographic maps, which show variations in neuron density across the retina. Although topographic maps of about 300 vertebrates are available, there is no method for characterizing retinal traits quantitatively. Our goal is to present a novel method to standardize information on the position of the retinal specializations and changes in retinal ganglion cell (RGC) density across the retina from published topographic maps. We measured the position of the retinal specialization using two Cartesian coordinates and the gradient in cell density by sampling ganglion cell density values along four axes (nasal, temporal, ventral, and dorsal). Using this information, along with the peak and lowest RGC densities, we conducted discriminant function analyses (DFAs) to establish if this method is sensitive to distinguish three common types of retinal specializations (fovea, area, and visual streak). The discrimination ability of the model was higher when considering terrestrial (78%-80% correct classification) and aquatic (77%-86% correct classification) species separately than together. Our method can be used in the future to test specific hypotheses on the differences in retinal morphology between retinal specializations and the association between retinal morphology and behavioral and ecological traits using comparative methods controlling for phylogenetic effects.

Anatomical specializations for nocturnality in a critically endangered parrot, the Kakapo (Strigops habroptilus).

The shift from a diurnal to nocturnal lifestyle in vertebrates is generally associated with either enhanced visual sensitivity or a decreased reliance on vision. Within birds, most studies have focused on differences in the visual system across all birds with respect to nocturnality-diurnality. The critically endangered Kakapo (Strigops habroptilus), a parrot endemic to New Zealand, is an example of a species that has evolved a nocturnal lifestyle in an otherwise diurnal lineage, but nothing is known about its' visual system. Here, we provide a detailed morphological analysis of the orbits, brain, eye, and retina of the Kakapo and comparisons with other birds. Morphometric analyses revealed that the Kakapo's orbits are significantly more convergent than other parrots, suggesting an increased binocular overlap in the visual field. The Kakapo exhibits an eye shape that is consistent with other nocturnal birds, including owls and nightjars, but is also within the range of the diurnal parrots. With respect to the brain, the Kakapo has a significantly smaller optic nerve and tectofugal visual pathway. Specifically, the optic tectum, nucleus rotundus and entopallium were significantly reduced in relative size compared to other parrots. There was no apparent reduction to the thalamofugal visual pathway. Finally, the retinal morphology of the Kakapo is similar to that of both diurnal and nocturnal birds, suggesting a retina that is specialised for a crepuscular niche. Overall, this suggests that the Kakapo has enhanced light sensitivity, poor visual acuity and a larger binocular field than other parrots. We conclude that the Kakapo possesses a visual system unlike that of either strictly nocturnal or diurnal birds and therefore does not adhere to the traditional view of the evolution of nocturnality in birds.

Retinogeniculostriate pathway components scale with orbit convergence only in primates and not in other mammals.

Studies of the relative sizes of brain components in mammals suggest that areas responsible for sensory processing, including visual processing, are correlated with aspects of ecology, especially activity pattern. Some studies suggest that primate orbit convergence and binocular vision are correlated with the overall size of the brain as well as components of the visual pathway, such as the lateral geniculate nucleus. However, the question remains whether components of the visual pathway are correlated with orbit convergence and binocular visual field overlap in nonprimate mammals. Here, we examine the relationship between orbit convergence and the volumes of components of the visual pathway (optic tract, dorsal lateral geniculate nucleus and primary visual cortex). Data on orbit orientation are combined with those on overall brain volume as well as brain component volumes in a taxonomically diverse sample of mammals. Our results demonstrate that nonprimate mammals scale isometrically for component volumes along the visual pathway, whereas primates display negatively allometric relationships. However, only among primates is higher orbit convergence correlated with volumetrically larger lateral geniculate nuclei and visual cortices. Diurnal primates exhibit statistically larger visual pathway components when compared to nocturnal primates. Nonprimate mammals do not display activity pattern differences with the single exception of optic tract sizes. We conclude that binocular vision was a much stronger factor in the evolution of the visual system in primates than in other mammals.

The nocturnal bottleneck and the evolution of mammalian vision.

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.

Relative Wulst volume is correlated with orbit orientation and binocular visual field in birds.

In mammals, species with more frontally oriented orbits have broader binocular visual fields and relatively larger visual regions in the brain. Here, we test whether a similar pattern of correlated evolution is present in birds. Using both conventional statistics and modern comparative methods, we tested whether the relative size of the Wulst and optic tectum (TeO) were significantly correlated with orbit orientation, binocular visual field width and eye size in birds using a large, multi-species data set. In addition, we tested whether relative Wulst and TeO volumes were correlated with axial length of the eye. The relative size of the Wulst was significantly correlated with orbit orientation and the width of the binocular field such that species with more frontal orbits and broader binocular fields have relatively large Wulst volumes. Relative TeO volume, however, was not significant correlated with either variable. In addition, both relative Wulst and TeO volume were weakly correlated with relative axial length of the eye, but these were not corroborated by independent contrasts. Overall, our results indicate that relative Wulst volume reflects orbit orientation and possibly binocular visual field, but not eye size.

Ecomorphology of orbit orientation and the adaptive significance of binocular vision in primates and other mammals.

Primates are characterized by forward-facing, or convergent, orbits and associated binocular field overlap. Hypotheses explaining the adaptive significance of these traits often relate to ecological factors, such as arboreality, nocturnal visual predation, or saltatory locomotion in a complex nocturnal, arboreal environment. This study re-examines the ecological factors that are associated with high orbit convergence in mammals. Orbit orientation data were collected for 321 extant taxa from sixteen orders of metatherian (marsupial) and eutherian mammals. These taxa were coded for activity pattern, degree of faunivory, and substrate preference. Results demonstrate that nocturnal and cathemeral mammals have significantly more convergent orbits than diurnal taxa, both within and across orders. Faunivorous eutherians (both nocturnal and diurnal) have higher mean orbit convergence than opportunistically foraging or non-faunivorous taxa. However, substrate preference is not associated with higher orbit convergence and, by extension, greater binocular visual field overlap. These results are consistent with the hypothesis that mammalian predators evolved higher orbit convergence, binocular vision, and stereopsis to counter camouflage in prey inhabiting a nocturnal environment. Strepsirhine primates have a range of orbit convergence values similar to nocturnal or cathemeral predatory non-primate mammals. These data are entirely consistent with the nocturnal visual predation hypothesis of primate origins.

Malagasy primate origins: phylogenies, fossils, and biogeographic reconstructions.

The geographic origin of Malagasy primates is a rich source of debate, providing a useful context for understanding effects of differing phylogenetic interpretations upon area of origin reconstructions. This study has evaluated the biogeographic implications of competing primate phylogenies in order to reconstruct the area of origin of Malagasy strepsirhines. The robusticity of biogeographic inference is examined based on sensitivity to tree topology. The results demonstrate extreme vulnerability to both out-group choice and internal tree topology, suggesting caution for area of origin interpretations from phylogenies that exclude fossil taxa. Moreover, even a single taxon can have a powerful effect upon biogeographic interpretations. Perhaps not surprisingly, it is only with greater phylogenetic resolution that a clearer understanding of the biogeographic origins of Malagasy primates will emerge.

Function of the mammalian postorbital bar.

Complete postorbital bars, bony arches that encompass the lateral aspect of the eye and form part of a circular orbit, have evolved homoplastically multiple times during mammalian evolution. Numerous functional hypotheses have been advanced for postorbital bars, the most promising being that postorbital bars function to stiffen the lateral orbit in taxa that have significant angular deviation between the temporal fossa and the bony orbit. Without a stiff lateral orbit the anterior temporalis muscle and fascia potentially would pull on the postorbital ligament, deform the orbit, and cause disruption of oculomotor precision. Morphometric data were collected on 1,329 specimens of 324 taxa from 16 orders of extant eutherian and metatherian mammals in order to test whether the orientation of the orbit relative to the temporal fossa is correlated with the replacement of the postorbital ligament with bone. The allometric and ecological influences on orbit orientation across mammals are also explored. The morphometric results corroborate the hypothesis: Shifts in orbit orientation relative to the temporal fossa are correlated with the size of the postorbital processes, which replace the ligament. The allometric and ecological factors that influence orbit orientation vary across taxa. Postorbital bars stiffen the lateral orbital wall. Muscle pulleys, ligaments, and other connective tissue attach to the lateral orbital wall, including the postorbital bar. Without a stiff lateral orbit, deformation due to temporalis contraction would displace soft tissues contributing to normal oculomotor function.

On the relationship between orbit orientation and binocular visual field overlap in mammals.

The orbital apertures of Primates are among the most convergent (i.e., facing in the same direction) among mammals. It is often assumed that orbit convergence is associated with binocular visual field overlap and stereoscopic depth perception in primates. Likewise, it is also assumed that orbit orientation reflects the shape of the visual field across mammals. To date, however, no study has demonstrated that orbit and visual field orientation are correlated, much less comparable, across mammals. In this study, data on orbit convergence were collected for a representative sample of mammals for which data on the extent of the visual field are available. Both standard and phylogenetically controlled comparisons were made. The results demonstrate that orbit convergence and binocular visual field overlap are significantly correlated and display a linear relationship. Based on orbit convergence, Primates as a group have the largest binocular visual fields among mammals.