The complex evolution of primate color vision has puzzled biologists for decades. Primates are the only eutherian mammals that evolved an enhanced capacity for discriminating colors in the green-red part of the spectrum (trichromatism). However, while Old World primates present three types of cone pigments and are routinely trichromatic, most New World primates exhibit a color vision polymorphism, characterized by the occurrence of trichromatic and dichromatic females and obligatory dichromatic males. Even though this has stimulated a prolific line of inquiry, the selective forces and relative benefits influencing color vision evolution in primates are still under debate, with current explanations focusing almost exclusively at the advantages in finding food and detecting socio-sexual signals. Here, we evaluate a previously untested possibility, the adaptive value of primate color vision for predator detection. By combining color vision modeling data on New World and Old World primates, as well as behavioral information from human subjects, we demonstrate that primates exhibiting better color discrimination (trichromats) excel those displaying poorer color visions (dichromats) at detecting carnivoran predators against the green foliage background. The distribution of color vision found in extant anthropoid primates agrees with our results, and may be explained by the advantages of trichromats and dichromats in detecting predators and insects, respectively.
Primate color vision is based on two to three cone types in the retina, each expressing a different class of visual pigment, making them the only mammals that possess trichromacy. These pigment classes are the short wavelength-sensitive (SWS1) pigment and the long wavelength-sensitive (LWS) pigment, orthologues of the same pigments found in many other vertebrates, as well as the middle wavelength-sensitive (MWS) pigment, a paralogue to the LWS pigment. Trichromacy was achieved differently in Old World and New World primates. In Old World primates, a duplication of the LWS opsin gene occurred giving rise to a "red-sensitive" or L pigment and a "green-sensitive" or M pigment. Their corresponding L and M genes are adjacent on the X chromosome which, together with their high sequence homology, is the underlying cause for the high frequency of red-green color blindness seen in humans. In New World primates and prosimians, however, the mechanism leading to trichromacy, with one exception, is based on a single polymorphic LWS gene, from which different allelic variants encode pigments with differing spectral peaks. X chromosome inactivation limits expression to just one gene per photoreceptor meaning that trichromacy is only seen in females; while all male are red-green color blind. Despite several leading hypotheses, the reasons for the different evolutionary paths taken by Old and New World primates for trichromacy are still unclear and remain to be confirmed.
Among placental mammals, only primates have trichromatic color vision, however this is not a uniform condition. Under different genetic status, Old World monkeys have routine trichromacy, while New World monkeys show a visual polymorphism, characterized by obligatory male dichromacy. The ecological role of this genetic difference still remains unclear, but some studies show that dichromats and trichromats appear to have different abilities in detecting colored targets against a background of leaves. The Cerrado's marmoset (Callithrix penicillata) is known to forage in brightly illuminated (savanna-like vegetation) and dimly illuminated (forests) environments, exploiting a high amount of dark fruits. Hence, it seems to be a good model for studying the differential advantages enjoyed by each color vision phenotype under natural conditions. Our aim was to verify how the different phenotypes of Cerrado's marmoset detect components of their diet, evaluating the existence of differential phenotype advantages. Under two different light conditions, visual signals of naturally consumed fruits were modeled against different backgrounds scenarios. Even though dichromats and trichromats appear to be equally suited for tasks involving fruit detection, phenotype differential advantages are observed in this marmoset. In many conditions trichromats are predicted to perform better than dichromats, but under low ambient light dichromats manage to outperform trichromats in some scenarios. Phenotypes that carry widely spaced and longer M/L pigments enjoy the most advantage. These differential performances of trichromatic phenotypes, together with overdominance selection, seem to explain the maintenance of the tri-allelic system found in callitrichids.
Bats are a diverse radiation of mammals of enduring interest for understanding the evolution of sensory specialization. Colour vision variation among species has previously been linked to roosting preferences and echolocation form in the suborder Yinpterochiroptera, yet questions remain about the roles of diet and habitat in shaping bat visual ecology. We sequenced OPN1SW and OPN1LW opsin genes for 20 species of leaf-nosed bats (family Phyllostomidae; suborder Yangochiroptera) with diverse roosting and dietary ecologies, along with one vespertilionid species (Myotis lavali). OPN1LW genes appear intact for all species, and predicted spectral tuning of long-wavelength opsins varied among lineages. OPN1SW genes appear intact and under purifying selection for Myotis lavali and most phyllostomid bats, with two exceptions: (a) We found evidence of ancient OPN1SW pseudogenization in the vampire bat lineage, and loss-of-function mutations in all three species of extant vampire bats; (b) we additionally found a recent, independently derived OPN1SW pseudogene in Lonchophylla mordax, a cave-roosting species. These mutations in leaf-nosed bats are independent of the OPN1SW pseudogenization events previously reported in Yinpterochiropterans. Therefore, the evolution of monochromacy (complete colour blindness) has occurred in both suborders of bats and under various evolutionary drivers; we find independent support for the hypothesis that obligate cave roosting drives colour vision loss. We additionally suggest that haematophagous dietary specialization and corresponding selection on nonvisual senses led to loss of colour vision through evolutionary sensory trade-off. Our results underscore the evolutionary plasticity of opsins among nocturnal mammals.
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