Anatomy and dietary specialization influence sensory behaviour among sympatric primates.

Senses form the interface between animals and environments, and provide a window into the ecology of past and present species. However, research on sensory behaviours by wild frugivores is sparse. Here, we examine fruit assessment by three sympatric primates (Alouatta palliata, Ateles geoffroyi and Cebus imitator) to test the hypothesis that dietary and sensory specialization shape foraging behaviours. Ateles and Cebus groups are comprised of dichromats and trichromats, while all Alouatta are trichomats. We use anatomical proxies to examine smell, taste and manual touch, and opsin genotyping to assess colour vision. We find that the frugivorous spider monkeys (Ateles geoffroyi) sniff fruits most often, omnivorous capuchins (Cebus imitator), the species with the highest manual dexterity, use manual touch most often, and that main olfactory bulb volume is a better predictor of sniffing behaviour than nasal turbinate surface area. We also identify an interaction between colour vision phenotype and use of other senses. Controlling for species, dichromats sniff and bite fruits more often than trichromats, and trichromats use manual touch to evaluate cryptic fruits more often than dichromats. Our findings reveal new relationships among dietary specialization, anatomical variation and foraging behaviour, and promote understanding of sensory system evolution.

The sensory ecology of primate food perception, revisited.

Twenty years ago, Dominy and colleagues published "The sensory ecology of primate food perception," an impactful review that brought new perspectives to understanding primate foraging adaptations. Their review synthesized information on primate senses and explored how senses informed feeding behavior. Research on primate sensory ecology has seen explosive growth in the last two decades. Here, we revisit this important topic, focusing on the numerous new discoveries and lines of innovative research. We begin by reviewing each of the five traditionally recognized senses involved in foraging: audition, olfaction, vision, touch, and taste. For each sense, we provide an overview of sensory function and comparative ecology, comment on the state of knowledge at the time of the original review, and highlight advancements and lingering gaps in knowledge. Next, we provide an outline for creative, multidisciplinary, and innovative future research programs that we anticipate will generate exciting new discoveries in the next two decades.

Potential arms race in the coevolution of primates and angiosperms: brazzein sweet proteins and gorilla taste receptors.

OBJECTIVES: We explored whether variation in the sweet taste receptor protein T1R3 in primates could contribute to differences in sweet taste repertoire among species, potentially reflecting coevolution with local plants. Specifically, we examined which primates are likely to be sweet "tasters" of brazzein, a protein found in the fruit of the African plant Pentadiplandra brazzeana that tastes intensely sweet to humans, but provides little energy. Sweet proteins like brazzein are thought to mimic the taste of sugars to entice seed dispersers. We examined the evolution of T1R3 and assessed whether primates are likely "deceived" by such biochemical mimicry. METHODS: Using published and new sequence data for TAS1R3, we characterized 57 primates and other mammals at the two amino acid sites necessary to taste brazzein to determine which species are tasters. We further used dN/dS-based methods to look for statistical evidence of accelerated evolution in this protein across primate lineages. RESULTS: The taster genotype is shared across most catarrhines, suggesting that most African primates can be "tricked" into eating and dispersing P. brazzeana's seeds for little caloric gain. Western gorillas (Gorilla gorilla), however, exhibit derived mutations at the two brazzein-critical positions, and although fruit is a substantial portion of the western gorilla diet, they have not been observed to eat P. brazzeana. Our analyses of protein evolution found no signature of positive selection on TAS1R3 along the gorilla lineage. DISCUSSION: We propose that the gorilla-specific mutations at the TAS1R3 locus encoding T1R3 could be a counter-adaptation to the false sweet signal of brazzein.

Nocturnal light environments influence color vision and signatures of selection on the OPN1SW opsin gene in nocturnal lemurs.

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.

Visual acuity in mammals: effects of eye size and ecology.

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.

Human subsistence and signatures of selection on chemosensory genes.

Chemosensation (olfaction, taste) is essential for detecting and assessing foods, such that dietary shifts elicit evolutionary changes in vertebrate chemosensory genes. The transition from hunting and gathering to agriculture dramatically altered how humans acquire food. Recent genetic and linguistic studies suggest agriculture may have precipitated olfactory degeneration. Here, we explore the effects of subsistence behaviors on olfactory (OR) and taste (TASR) receptor genes among rainforest foragers and neighboring agriculturalists in Africa and Southeast Asia. We analyze 378 functional OR and 26 functional TASR genes in 133 individuals across populations in Uganda (Twa, Sua, BaKiga) and the Philippines (Agta, Mamanwa, Manobo) with differing subsistence histories. We find no evidence of relaxed selection on chemosensory genes in agricultural populations. However, we identify subsistence-related signatures of local adaptation on chemosensory genes within each geographic region. Our results highlight the importance of culture, subsistence economy, and drift in human chemosensory perception.

Nocturnal light environments and species ecology: implications for nocturnal color vision in forests.

Although 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 (r=0.85, 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 560 nm. 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 (P=0.002). These results suggest that variation in nocturnal light environments and species ecology together influence cone spectral tuning and color vision in nocturnal mammals.

Color vision and niche partitioning in a diverse neotropical primate community in lowland Amazonian Ecuador.

A recent focus in community ecology has been on how within-species variability shapes interspecific niche partitioning. Primate color vision offers a rich system in which to explore this issue. Most neotropical primates exhibit intraspecific variation in color vision due to allelic variation at the middle-to-long-wavelength opsin gene on the X chromosome. Studies of opsin polymorphisms have typically sampled primates from different sites, limiting the ability to relate this genetic diversity to niche partitioning. We surveyed genetic variation in color vision of five primate species, belonging to all three families of the primate infraorder Platyrrhini, found in the Yasuní Biosphere Reserve in Ecuador. The frugivorous spider monkeys and woolly monkeys (Ateles belzebuth and Lagothrix lagotricha poeppigii, family Atelidae) each had two opsin alleles, and more than 75% of individuals carried the longest-wavelength (553-556 nm) allele. Among the other species, Saimiri sciureus macrodon (family Cebidae) and Pithecia aequatorialis (family Pitheciidae) had three alleles, while Plecturocebus discolor (family Pitheciidae) had four alleles-the largest number yet identified in a wild population of titi monkeys. For all three non-atelid species, the middle-wavelength (545 nm) allele was the most common. Overall, we identified genetic evidence of fourteen different visual phenotypes-seven types of dichromats and seven trichromats-among the five sympatric taxa. The differences we found suggest that interspecific competition among primates may influence intraspecific frequencies of opsin alleles. The diversity we describe invites detailed study of foraging behavior of different vision phenotypes to learn how they may contribute to niche partitioning.

Opsin gene polymorphism predicts trichromacy in a cathemeral lemur.

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.

Visual acuity in the cathemeral strepsirrhine Eulemur macaco flavifrons.

Studies of visual acuity in primates have shown that diurnal haplorhines have higher acuity (30-75 cycles per degree (c/deg)) than most other mammals. However, relatively little is known about visual acuity in non-haplorhine primates, and published estimates are only available for four strepsirrhine genera (Microcebus, Otolemur, Galago, and Lemur). We present here the first measurements of visual acuity in a cathemeral strepsirrhine species, the blue-eyed black lemur (Eulemur macaco flavifrons). Acuity in two subjects, a 3-year-old male and a 16-year-old female, was assessed behaviorally using a two-alternative forced choice discrimination task. Visual stimuli consisted of high contrast square wave gratings of seven spatial frequencies. Acuity threshold was determined using a 70% correct response criterion. Results indicate a maximum visual acuity of 5.1 c/deg for the female (1718 trials) and 3.8 c/deg for the male (846 trials). These values for E. macaco are slightly lower than those reported for diurnal Lemur catta, and are generally comparable to those reported for nocturnal Microcebus murinus and Otolemur crassicaudatus. To examine ecological sources of variation in primate visual acuity, we also calculated maximum theoretical acuity for Cheirogaleus medius (2.8 c/deg) and Tarsius syrichta (8.9 c/deg) using published data on retinal ganglion cell density and eye morphology. These data suggest that visual acuity in primates may be influenced by activity pattern, diet, and phylogenetic history. In particular, the relatively high acuity of T. syrichta and Galago senegalensis suggests that visual predation may be an important selective factor favoring high visual acuity in primates.

Group benefit associated with polymorphic trichromacy in a Malagasy primate (Propithecus verreauxi).

In some primate lineages, polymorphisms in the X-linked M/LWS opsin gene have produced intraspecific variation in color vision. In these species, heterozygous females exhibit trichromacy, while males and homozygous females exhibit dichromacy. The evolutionary persistence of these polymorphisms suggests that balancing selection maintains color vision variation, possibly through a 'trichromat advantage' in detecting yellow/orange/red foods against foliage. We identified genetic evidence of polymorphic trichromacy in a population of Verreaux's sifaka (Propithecus verreauxi) at Kirindy Mitea National Park in Madagascar, and explored effects of color vision on reproductive success and feeding behavior using nine years of morphological, demographic, and feeding data. We found that trichromats and dichromats residing in social groups with trichromats exhibit higher body mass indices than individuals in dichromat-only groups. Additionally, individuals in a trichromat social group devoted significantly more time to fruit feeding and had longer fruit feeding bouts than individuals in dichromat-only groups. We hypothesize that, due to small, cohesive sifaka social groups, a trichromat advantage in detecting productive fruit patches during the energetically stressful dry season also benefits dichromats in a trichromat's group. Our results offer the first support for the 'mutual benefit of association' hypothesis regarding the maintenance of polymorphic trichromacy in primates.

Effects of habitat light intensity on mammalian eye shape.

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.