Diet and the evolution of ADH7 across seven orders of mammals.

Dietary variation within and across species drives the eco-evolutionary responsiveness of genes necessary to metabolize nutrients and other components. Recent evidence from humans and other mammals suggests that sugar-rich diets of floral nectar and ripe fruit have favoured mutations in, and functional preservation of, the ADH7 gene, which encodes the ADH class 4 enzyme responsible for metabolizing ethanol. Here we interrogate a large, comparative dataset of ADH7 gene sequence variation, including that underlying the amino acid residue located at the key site (294) that regulates the affinity of ADH7 for ethanol. Our analyses span 171 mammal species, including 59 newly sequenced. We report extensive variation, especially among frugivorous and nectarivorous bats, with potential for functional impact. We also report widespread variation in the retention and probable pseudogenization of ADH7. However, we find little statistical evidence of an overarching impact of dietary behaviour on putative ADH7 function or presence of derived alleles at site 294 across mammals, which suggests that the evolution of ADH7 is shaped by complex factors. Our study reports extensive new diversity in a gene of longstanding ecological interest, offers new sources of variation to be explored in functional assays in future study, and advances our understanding of the processes of molecular evolution.

The effect of pelage, background, and distance on predator detection and the evolution of primate color vision.

Primates' predators, such as carnivore mammals, usually rely on camouflage to increase proximity to prey and start a predatory attempt. Camouflage depends not only on the color pattern presented by a predator's pelage but also on the background scene in which the hunting takes place. Another factor that influences camouflage effectiveness is prey's color vision since a given camouflage strategy might not work for all visual phenotypes. Still, little research has been made on the effect of primate visual phenotype on predator detection. Here, we investigate the effects of natural pelages, background scenarios, visual phenotypes, and detection distances on predator detection. We used photographs of taxidermized carnivores (ocelots, cougars, and lesser grisons) as detection stimuli, taken in three different natural scenarios (forest, savanna, and grassland), and at two viewing distances (near and far). On a touchscreen monitor, sets of four images (only one containing a hidden animal) were randomly presented to 39 human males (19 dichromats and 20 trichromats). We found that trichromats, when compared to dichromats, present a lower latency and a higher accuracy of carnivore detection for some conditions tested. We also found that pelage color, background scenario, and detection distance interact to influence the effectiveness of camouflage. Our results suggest that trichromacy might be even more advantageous for carnivore detection than thought before, since it facilitates detection of mammals with diverse pelage colorations, in environments with different phytophysiognomies, and at longer distances. We also propose that the higher rates of dichromacy found in modern human societies could have resulted from a relaxation in predation.

Genetic variability of the sws1 cone opsin gene among New World monkeys.

Vision is a major sense for Primates and the ability to perceive colors has great importance for the species ecology and behavior. Visual processing begins with the activation of the visual opsins in the retina, and the spectral absorption peaks are highly variable among species. In most Primates, LWS/MWS opsins are responsible for sensitivity to long/middle wavelengths within the visible light spectrum, and SWS1 opsins provide sensitivity to short wavelengths, in the violet region of the spectrum. In this study, we aimed to investigate the genetic variation on the sws1 opsin gene of New World monkeys (NWM) and search for amino acid substitutions that might be associated with the different color vision phenotypes described for a few species. We sequenced the exon 1 of the sws1 opsin gene of seven species from the families Callitrichidae, Cebidae, and Atelidae, and searched for variation at the spectral tuning sites 46, 49, 52, 86, 90, 93, 114, 116, and 118. Among the known spectral tuning sites, only residue 114 was variable. To investigate whether other residues have a functional role in the SWS1 absorption peak, we performed computational modeling of wild-type SWS1 and mutants A50I and A50V, found naturally among the species investigated. Although in silico analysis did not show any visible effect caused by these substitutions, it is possible that interactions of residue 50 with other sites might have some effect in the spectral shifts in the order of ~14 nm, found among the NWM. We also performed phylogenetic reconstruction of the sws1 gene, which partially recovered the species phylogeny. Further studies will be important to uncover the mutations responsible for the phenotypic variability of the SWS1 of NWM, and how spectral tuning may be associated with specific ecological features such as preferred food items and habitat use.

Detection of insect prey by wild common marmosets: The effect of color vision.

Most species of New World primates have an unusual color vision pattern that can affect an individual's ability to detect food. Whereas males can only be dichromatic, females can be either dichromatic or trichromatic. Trichromats are expected to have an advantage in detecting conspicuous food whereas dichromats should be better at locating cryptic resources. Here we aimed to understand how color vision phenotype influences insect foraging by five groups of common marmosets living in a semiarid environment. We recorded insect predation events, noting morphotype and color of the captured insect, and the substrate from which it was captured. Color modeling suggested that, for all values of chromatic contrast resulting from comparing the measured insect-substrate pairs, trichromats outperformed dichromats. Females showed an overall higher insect capture rate than males. Females also showed a higher capture rate of conspicuous insects but there was no sex difference for the capture of cryptic insects. When we compared only dichromatic individuals there was no difference between sexes. These findings suggest that differences found in capture rate related not only to sex but also to visual polymorphism and that the latter is a crucial factor determining insect capture rate in common marmosets. Nevertheless, these results should be interpreted with caution because of the small number (three) of dichromat females and the unknown phenotype of the remaining females. Our results support the balancing selection hypothesis, suggesting that the advantage of one phenotype over the other may depend on environmental circumstances. This hypothesis has recently been considered as the most plausible for the maintenance of visual polymorphism in New World primates.

Colour vision variation in leaf-nosed bats (Phyllostomidae): Links to cave roosting and dietary specialization.

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.

Female Brazilian whiptail lizards (Cnemidophorus ocellifer) prefer males with high ultraviolet ornament reflectance.

Conspicuous colouration is an important way of social communication in many taxa. The role of ultraviolet (UV) signals in intraspecific communication has only recently been studied in lizards, and there is not a general understanding of the adaptive role of UV colouration. Colour ornaments can signal male quality in mate choice and are therefore suitable for reliably predicting the outcome of female preference. Here, we tested the potential role of UV colouration in female spatial preference in a non-territorial teiid lizard, Cnemidophorus ocellifer. We experimentally manipulated the UV reflectance of size-matched male pairs and tested the effects of our treatment on females' spatial distribution. We found that females associated with males of higher UV reflectance, suggesting that UV colour can be an important clue during mate preference decisions. Our results provide the first empirical evidence for the importance of UV colouration in female preference in a mutually ornamented lizard species.

Effect of light intensity on food detection in captive great fruit-eating bats, Artibeus lituratus (Chiroptera: Phyllostomidae).

Bats are known for their well-developed echolocation. However, several experiments focused on the bat visual system have shown evidence of the importance of visual cues under specific luminosity for different aspects of bat biology, including foraging behavior. This study examined the foraging abilities of five female great fruit-eating bats, Artibeus lituratus, under different light intensities. Animals were given a series of tasks to test for discrimination between a food target against an inedible background, under light levels similar to the twilight illumination (18lx), the full moon (2lx) and complete darkness (0lx). We found that the bats required a longer time frame to detect targets under a light intensity similar to twilight, possibly due to inhibitory effects present under a more intense light level. Additionally, bats were more efficient at detecting and capturing targets under light conditions similar to the luminosity of a full moon, suggesting that visual cues were important for target discrimination. These results demonstrate that light intensity affects foraging behavior and enables the use of visual cues for food detection in frugivorous bats. This article is part of a Special Issue entitled: Neotropical Behaviour.

Behavioural evidence of sex-linked colour vision polymorphism in the squirrel monkey Saimiri ustus.

Squirrel monkeys, like most Neotropical primates, display a sex-linked colour vision polymorphism. Here we assess the colour perception of 8 Saimiri ustus by a behavioural paradigm using Munsell colour chips as discriminating stimuli. A random variation in brightness assured that discriminations were based on colour rather than brightness cues. Results indicate that all males showed random performances when presented with stimuli which, in previous experiments with human colour-blind individuals and dichromatic non-human primates, proved to be difficult to discriminate. Females behaved as trichromats. The different phenotypes in S. ustus may offer diverse advantages in feeding ecology and are in agreement with the existence of vision polymorphism, as described for other species of squirrel monkeys.

Influence of stimuli size on color discrimination in capuchin monkeys.

Large-field trichromacy is a general feature of protanope and deuteranope humans, provided that the stimuli size extends to an 8 degrees visual angle. In this study we compared the performance of five male and three female tufted capuchin monkeys (Cebus apella) in discriminating pairs of Munsell color papers. Human subjects were also studied in two-choice discrimination tests, using the same stimuli and apparatus employed for the monkeys. The results show that although the dichromatic humans showed improved discrimination with larger versions of the stimuli, the dichromatic monkeys exhibited the same performance for both stimuli sizes. Thus, Cebus apella apparently do not present large-field trichromacy-at least for the conditions in the present experiments.

Color vision in marmosets and tamarins: behavioral evidence.

Here we demonstrate differences in the relative performance of 15 callitrichids tested in a series of color visual discrimination experiments. Munsell color chips were chosen as stimuli based on their use in earlier experiments with human dichromats. We show behavioral evidence for the existence of four distinct kinds of color-vision phenotypes, each of which has slightly different color discrimination abilities. The different phenotypes may offer different advantages. The data are in accordance with the existence of a visual polymorphism in callitrichids.

Colour discrimination in the black-tufted-ear marmoset (Callithrix penicillata): ecological implications.

The dietary diversity of marmosets is substantial, which may reflect differences in their colour vision. This study examined the colour discrimination ability of a gummivore/insectivore callitrichid, Callithrix penicillata, which inhabits the Brazilian cerrado (bush savanna). A series of ecologically relevant tasks, involving a behavioural paradigm of discrimination learning in semi-natural conditions and the usage of ecologically relevant stimuli, was executed. Three marmosets, 2 males and a female, behaved like human dichromats, showing an impaired performance when orange and green stimuli had to be discriminated. In contrast, 2 females resembled human trichromats, discriminating those kinds of pairs. Our data suggest that Callithrix penicillata presents a polymorphic trichromacy, with dichromatic males and dichromatic or trichromatic females.

Colour discrimination learning in black-handed tamarin ( Saguinus midas niger).

Colour is one cue that monkeys use for perceptual segregation of targets and to identify food resources. For fruit-eating primates such as Saguinus, an accurate colour perception would be advantageous to help find ripe fruits at distance. The colour vision abilities of black-handed tamarins ( Saguinus midas niger) were assessed through a discrimination learning paradigm using Munsell colour chips as stimuli. Pairs of chips were chosen from an early experiment with protan and deutan humans. The monkeys (three males and one female) were tested with stimuli of the same hue, but different brightness values, in order to make sure that discriminations were based on colour rather than brightness cues. The results showed that the female, but not the males, presented an above-chance performance for stimuli resembling hue conditions under which tamarins forage (oranges vs greens). Colour vision in S. m. niger is discussed according to the advantages and disadvantages of dichromatism in daily search for food as well as to aspects regarding polymorphism in New World monkeys.

Color vision perception in the capuchin monkey (Cebus apella): a re-evaluation of procedures using Munsell papers.

In previous experiments based on color vision discrimination of Munsell chips, Pessoa et al. (Behav Brain Res 1997;89:285-8) presented evidence of trichromatic color vision in capuchin monkeys. However, the possibility of subjects using brightness cues was not eliminated. The purpose of the present study was to reassess the color perception in Cebus apella in a similar behavioral paradigm, but using a range of brightness values at each tested hue. We now report that male capuchins show a dichromatic behavior. The results are discussed in terms of the hypothesis of male dichromatism in the New World monkey, the biological role of color vision and cognitive abilities of capuchin monkeys.