Previous comparative research has attributed interspecific variation in eye size among mammals to selection related to visual acuity. Mammalian species have also been hypothesized to differ in visual acuity partly as a result of differences in ecology. While a number of prior studies have explored ecological and phylogenetic effects on eye shape, a broad comparative analysis of the relationships between visual acuity, eye size and ecology in mammals is currently lacking. Here we use phylogenetic comparative methods to explore these relationships in a taxonomically and ecologically diverse sample of 91 mammal species. These data confirm that axial eye length and visual acuity are significantly positively correlated in mammals. This relationship conforms to expectations based on theoretical optics and prior analyses of smaller comparative samples. Our data also demonstrate that higher visual acuity in mammals is associated with: (1) diurnality and (2) predatory habits once the effects of eye size and phylogeny have been statistically controlled. These results suggest that interspecific variation in mammalian visual acuity is the result of a complex interplay between phylogenetic history, visual anatomy and ecology.
SUMMARYAlthough variation in the color of light in terrestrial diurnal and twilight environments has been well documented, relatively little work has examined the color of light in nocturnal habitats. Understanding the range and sources of variation in nocturnal light environments has important implications for nocturnal vision, particularly following recent discoveries of nocturnal color vision. In this study, we measured nocturnal irradiance in a dry forest/woodland and a rainforest in Madagascar over 34 nights. We found that a simple linear model including the additive effects of lunar altitude, lunar phase and canopy openness successfully predicted total irradiance flux measurements across 242 clear sky measurements (r0.85, P<0.0001). However, the relationship between these variables and spectral irradiance was more complex, as interactions between lunar altitude, lunar phase and canopy openness were also important predictors of spectral variation. Further, in contrast to diurnal conditions, nocturnal forests and woodlands share a yellow-green-dominant light environment with peak flux at 560nm. To explore how nocturnal light environments influence nocturnal vision, we compared photoreceptor spectral tuning, habitat preference and diet in 32 nocturnal mammals. In many species, long-wavelength-sensitive cone spectral sensitivity matched the peak flux present in nocturnal forests and woodlands, suggesting a possible adaptation to maximize photon absorption at night. Further, controlling for phylogeny, we found that fruit/flower consumption significantly predicted short-wavelength-sensitive cone spectral tuning in nocturnal mammals (P0.002). These results suggest that variation in nocturnal light environments and species ecology together influence cone spectral tuning and color vision in nocturnal mammals. Supplementary material available online at
Although loss of short-wavelength-sensitive (SWS) cones and dichromatic color vision in mammals has traditionally been linked to a nocturnal lifestyle, recent studies have identified variation in selective pressure for the maintenance of the OPN1SW opsin gene (and thus, potentially dichromacy) among nocturnal mammalian lineages. These studies hypothesize that purifying selection to retain SWS cones may be associated with a selective advantage for nocturnal color vision under certain ecological conditions. In this study, we explore the effect of nocturnal light environment on OPN1SW opsin gene evolution in a diverse sample of nocturnal lemurs (106 individuals, 19 species, and 5 genera). Using both phylogenetic and population genetic approaches, we test whether species from closed canopy rainforests, which are impoverished in short-wavelength light, have experienced relaxed selection compared with species from open canopy forests. We identify clear signatures of differential selection on OPN1SW by habitat type. Our results suggest that open canopy species generally experience strong purifying selection to maintain SWS cones. In contrast, closed canopy species experience weaker purifying selection or a relaxation of selection on OPN1SW. We also found evidence of nonfunctional OPN1SW genes in all Phaner species and in Cheirogaleus medius, implying at least three independent losses of SWS cones in cheirogaleids. Our results suggest that the evolution of color vision in nocturnal lemurs has been influenced by nocturnal light environment.
Recent research has identified polymorphic trichromacy in three diurnal strepsirrhines: Coquerel's sifaka (Propithecus coquereli), black and white ruffed lemurs (Varecia variegata), and red ruffed lemurs (V. rubra). Current hypotheses suggest that the transitions to diurnality experienced by Propithecus and Varecia were necessary precursors to their independent acquisitions of trichromacy. Accordingly, cathemeral lemurs are thought to lack the M/L opsin gene polymorphism necessary for trichromacy. In this study, the M/L opsin gene was sequenced in ten cathemeral blue-eyed black lemurs (Eulemur macaco flavifrons). This analysis identified a polymorphism identical to that of other trichromatic strepsirrhines at the critical amino acid position 285 in exon 5 of the M/L opsin gene. Thus, polymorphic trichromacy is likely present in at least one cathemeral Eulemur species, suggesting that strict diurnality is not necessary for trichromacy. The presence of trichromacy in E. m. flavifrons suggests that a re-evaluation of current hypotheses regarding the evolution of strepsirrhine trichromacy may be necessary. Although the M/L opsin polymorphism may have been independently acquired three times in the lemurid-indriid clade, the distribution of opsin alleles in lemurids and indriids may also be consistent with a common origin of trichromacy in the last common ancestor of either the lemurids or the lemurid-indriid clade.
Many aspects of mammalian visual anatomy vary with activity pattern, reflecting the divergent selective pressures imposed by low light and high light visual environments. However, ambient light intensity can also differ substantially between and within habitats due to differences in foliage density. We explored the effects of interhabitat and intrahabitat variation in light intensity on mammalian visual anatomy. Data on relative cornea size, activity pattern, and habitat type were collected from the literature for 209 terrestrial mammal species. In general, mammalian relative cornea size significantly varied by habitat type. In within-order and across-mammal analyses, diurnal and cathemeral mammals from forested habitats exhibited relatively larger corneas than species from more open habitats, reflecting an adaptation to increase visual sensitivity in forest species. However, in all analyses, we found no habitat-type effect in nocturnal species, suggesting that nocturnal mammals may experience selection to maximize visual sensitivity across all habitats. We also examined whether vertical strata usage affected relative cornea size in anthropoid primates. In most analyses, species occupying lower levels of forests and woodlands did not exhibit relatively larger corneas than species utilizing higher levels. Thus, unlike differences in intensity between habitat types, differences in light intensity between vertical forest strata do not appear to exert a strong selective pressure on visual morphology. These results suggest that terrestrial mammal visual systems reflect specializations for habitat variation in light intensity, and that habitat type as well as activity pattern have influenced mammalian visual evolution. Anat Rec, 294:905-914, 2011. V V C 2011 Wiley-Liss, Inc.
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