Considering the Influence of Nonadaptive Evolution on Primate Color Vision

Color vision in primates is variable across species, and it represents a rare trait in which the genetic mechanisms underlying phenotypic variation are fairly well-understood. Research on primate color vision has largely focused on adaptive explanations for observed variation, but it remains unclear why some species have trichromatic or polymorphic color vision while others are red-green color blind. Lemurs, in particular, are highly variable. While some species are polymorphic, many closely-related species are strictly dichromatic. We provide the first characterization of color vision in a wild population of red-bellied lemurs (Eulemur rubriventer, Ranomafana National Park, Madagascar) with a sample size (87 individuals; N_{X chromosomes} = 134) large enough to detect even rare variants (0.95 probability of detection at ≥ 3% frequency). By sequencing exon 5 of the X-linked opsin gene we identified opsin spectral sensitivity based on known diagnostic sites and found this population to be dichromatic and monomorphic for a long wavelength allele. Apparent fixation of this long allele is in contrast to previously published accounts of Eulemur species, which exhibit either polymorphic color vision or only the medium wavelength opsin. This unexpected result may represent loss of color vision variation, which could occur through selective processes and/or genetic drift (e.g., genetic bottleneck). To indirectly assess the latter scenario, we genotyped 55 adult red-bellied lemurs at seven variable microsatellite loci and used heterozygosity excess and M-ratio tests to assess if this population may have experienced a recent genetic bottleneck. Results of heterozygosity excess but not M-ratio tests suggest a bottleneck might have occurred in this red-bellied lemur population. Therefore, while selection may also play a role, the unique color vision observed in this population might have been influenced by a recent genetic bottleneck. These results emphasize the need to consider adaptive and nonadaptive mechanisms of color vision evolution in primates.     

Niche partitioning in a sympatric cryptic species complex

Competition theory states that multiple species should not be able to occupy the same niche indefinitely. Morphologically, similar species are expected to be ecologically alike and exhibit little niche differentiation, which makes it difficult to explain the co‐occurrence of cryptic species. Here, we investigated interspecific niche differentiation within a complex of cryptic bumblebee species that co‐occur extensively in the United Kingdom. We compared the interspecific variation along different niche dimensions, to determine how they partition a niche to avoid competitive exclusion. We studied the species B. cryptarum, B. lucorum, and B. magnus at a single location in the northwest of Scotland throughout the flight season. Using mitochondrial DNA for species identification, we investigated differences in phenology, response to weather variables and forage use. We also estimated niche region and niche overlap between different castes of the three species. Our results show varying levels of niche partitioning between the bumblebee species along three niche dimensions. The species had contrasting phenologies: The phenology of B. magnus was delayed relative to the other two species, while B. cryptarum had a relatively extended phenology, with workers and males more common than B. lucorum early and late in the season. We found divergent thermal specialisation: In contrast to B. cryptarum and B. magnus, B. lucorum worker activity was skewed toward warmer, sunnier conditions, leading to interspecific temporal variation. Furthermore, the three species differentially exploited the available forage plants: In particular, unlike the other two species, B. magnus fed predominantly on species of heather. The results suggest that ecological divergence in different niche dimensions and spatio‐temporal heterogeneity in the environment may contribute to the persistence of cryptic species in sympatry. Furthermore, our study suggests that cryptic species provide distinct and unique ecosystem services, demonstrating that morphological similarity does not necessarily equate to ecological equivalence.     

Evolutionary renovation of L/M opsin polymorphism confers a fruit discrimination advantage to ateline New World monkeys

New World monkeys exhibit prominent colour vision variation due to allelic polymorphism of the long‐to‐middle wavelength (L/M) opsin gene. The known spectral variation of L/M opsins in primates is broadly determined by amino acid composition at three sites: 180, 277 and 285 (the ‘three‐sites’ rule). However, two L/M opsin alleles found in the black‐handed spider monkeys (Ateles geoffroyi) are known exceptions, presumably due to novel mutations. The spectral separation of the two L/M photopigments is 1.5 times greater than expected based on the ‘three‐sites’ rule. Yet the consequence of this for the visual ecology of the species is unknown, as is the evolutionary mechanism by which spectral shift was achieved. In this study, we first examine L/M opsins of two other Atelinae species, the long‐haired spider monkeys (A. belzebuth) and the common woolly monkeys (Lagothrix lagotricha). By a series of site‐directed mutagenesis, we show that a mutation Y213D (tyrosine to aspartic acid at site 213) in the ancestral opsin of the two alleles enabled N294K, which occurred in one allele of the ateline ancestor and increased the spectral separation between the two alleles. Second, by modelling the chromaticity of dietary fruits and background leaves in a natural habitat of spider monkeys, we demonstrate that chromatic discrimination of fruit from leaves is significantly enhanced by these mutations. This evolutionary renovation of L/M opsin polymorphism in atelines illustrates a previously unappreciated dynamism of opsin genes in shaping primate colour vision.     

High functional diversity in deep‐sea fish communities and increasing intraspecific trait variation with increasing latitude

Variation in both inter‐ and intraspecific traits affects community dynamics, yet we know little regarding the relative importance of external environmental filters versus internal biotic interactions that shape the functional space of communities along broad‐scale environmental gradients, such as latitude, elevation, or depth. We examined changes in several key aspects of functional alpha diversity for marine fishes along depth and latitude gradients by quantifying intra‐ and interspecific richness, dispersion, and regularity in functional trait space. We derived eight functional traits related to food acquisition and locomotion and calculated seven complementary indices of functional diversity for 144 species of marine ray‐finned fishes along large‐scale depth (50–1200 m) and latitudinal gradients (29°–51° S) in New Zealand waters. Traits were derived from morphological measurements taken directly from footage obtained using Baited Remote Underwater Stereo‐Video systems and museum specimens. We partitioned functional variation into intra‐ and interspecific components for the first time using a PERMANOVA approach. We also implemented two tree‐based diversity metrics in a functional distance‐based context for the first time: namely, the variance in pairwise functional distance and the variance in nearest neighbor distance. Functional alpha diversity increased with increasing depth and decreased with increasing latitude. More specifically, the dispersion and mean nearest neighbor distances among species in trait space and intraspecific trait variability all increased with depth, whereas functional hypervolume (richness) was stable across depth. In contrast, functional hypervolume, dispersion, and regularity indices all decreased with increasing latitude; however, intraspecific trait variation increased with latitude, suggesting that intraspecific trait variability becomes increasingly important at higher latitudes. These results suggest that competition within and among species are key processes shaping functional multidimensional space for fishes in the deep sea. Increasing morphological dissimilarity with increasing depth may facilitate niche partitioning to promote coexistence, whereas abiotic filtering may be the dominant process structuring communities with increasing latitude.     

Characterization of opsin gene alleles affecting color vision in a wild population of titi monkeys (Callicebus brunneus)

The color vision of most platyrrhine primates is determined by alleles at the polymorphic X-linked locus coding for the opsin responsible for the middle- to long-wavelength (M/L) cone photopigment. Females who are heterozygous at the locus have trichromatic vision, whereas homozygous females and all males are dichromatic. This study characterized the opsin alleles in a wild population of the socially monogamous platyrrhine monkey Callicebus brunneus (the brown titi monkey), a primate that an earlier study suggests may possess an unusual number of alleles at this locus and thus may be a subject of special interest in the study of primate color vision. Direct sequencing of regions of the M/L opsin gene using feces-, blood-, and saliva-derived DNA obtained from 14 individuals yielded evidence for the presence of three functionally distinct alleles, corresponding to the most common M/L photopigment variants inferred from a physiological study of cone spectral sensitivity in captive Callicebus.     

Shift in competitive ability mediated by soil biota in an invasive plant

Understanding the shifts in competitive ability and its driving forces is key to predict the future of plant invasion. Changes in the competition environment and soil biota are two selective forces that impose remarkable influences on competitive ability. By far, evidence of the interactive effects of competition environment and soil biota on competitive ability of invasive species is rare. Here, we investigated their interactive effects using an invasive perennial vine, Mikania micrantha. The competitive performance of seven M. micrantha populations varying in their conspecific and heterospecific abundance were monitored in a greenhouse experiment, by manipulating soil biota (live and sterilized) and competition conditions (competition‐free, intraspecific, and interspecific competition). Our results showed that with increasing conspecific abundance and decreasing heterospecific abundance, (1) M. micrantha increased intraspecific competition tolerance and intra‐ vs. interspecific competitive ability but decreased interspecific competition tolerance; (2) M. micrantha increased tolerance of the negative soil biota effect; and (3) interspecific competition tolerance of M. micrantha was increasingly suppressed by the presence of soil biota, but intraspecific competition tolerance was less affected. These results highlight the importance of the soil biota effect on the evolution of competitive ability during the invasion process. To better control M. micrantha invasion, our results imply that introduction of competition‐tolerant native plants that align with conservation priorities may be effective where M. micrantha populations are long‐established and inferior in inter‐ vs. intraspecific competitive ability, whereas eradication may be effective where populations are newly invaded and fast‐growing.     

Is color data from citizen science photographs reliable for biodiversity research?

1. Color research continuously demands better methods and larger sample sizes. Citizen science (CS) projects are producing an ever‐growing geo‐ and time‐referenced set of photographs of organisms. These datasets have the potential to make a huge contribution to color research, but the reliability of these data need to be tested before widespread implementation.
2. We compared the difference between color extracted from CS photographs with that of color extracted from controlled lighting conditions (i.e., the current gold standard in spectrometry) for both birds and plants. First, we tested the ability of CS photographs to quantify interspecific variability by assessing > 9,000 CS photographs of 537 Australian bird species with controlled museum spectrometry data. Second, we tested the ability of CS photographs to quantify intraspecific variability by measuring petal color data for two plant species using seven methods/sources with varying levels of control.
3. For interspecific questions, we found that by averaging out variability through a large sample size, CS photographs capture a large proportion of across species variation in plumage color within the visual part of the spectrum (R² = 0.68–0.71 for RGB space and 0.72–0.77 for CIE‐LAB space). Between 12 and 14 photographs per species are necessary to achieve this averaging effect for interspecific studies. Unsurprisingly, the CS photographs taken with commercial cameras failed to capture information in the UV part of the spectrum. For intraspecific questions, decreasing levels of control increase the color variation but averaging larger sample sizes can partially mitigate this, aside from particular issues related to saturation and irregularities in light capture.
4. CS photographs offer a very large sample size across space and time which offers statistical power for many color research questions. This study shows that CS photographs contain data that lines up closely with controlled measurements within the visual spectrum if the sample size is large enough, highlighting the potential of CS photographs for both interspecific and intraspecific ecological or biological questions. With regard to analyzing color in CS photographs, we suggest, as a starting point, to measure multiple random points within the ROI of each photograph for both patterned and unpatterned patches and approach the recommended sample size of 12–14 photographs per species for interspecific studies. Overall, this study provides groundwork in analyzing the reliability of a novel method, which can propel the field of studying color forward.

     

Alouatta Trichromatic Color Vision: Cone Spectra and Physiological Responses Studied with Microspectrophotometry and Single Unit Retinal Electrophysiology

The howler monkeys (Alouatta sp.) are the only New World primates to exhibit routine trichromacy. Both males and females have three cone photopigments. However, in contrast to Old World monkeys, Alouatta has a locus control region upstream of each opsin gene on the X-chromosome and this might influence the retinal organization underlying its color vision. Post-mortem microspectrophotometry (MSP) was performed on the retinae of two male Alouatta to obtain rod and cone spectral sensitivities. The MSP data were consistent with only a single opsin being expressed in each cone and electrophysiological data were consistent with this primate expressing full trichromacy. To study the physiological organization of the retina underlying Alouatta trichromacy, we recorded from retinal ganglion cells of the same animals used for MSP measurements with a variety of achromatic and chromatic stimulus protocols. We found MC cells and PC cells in the Alouatta retina with similar properties to those previously found in the retina of other trichromatic primates. MC cells showed strong phasic responses to luminance changes and little response to chromatic pulses. PC cells showed strong tonic response to chromatic changes and small tonic response to luminance changes. Responses to other stimulus protocols (flicker photometry; changing the relative phase of red and green modulated lights; temporal modulation transfer functions) were also similar to those recorded in other trichromatic primates. MC cells also showed a pronounced frequency double response to chromatic modulation, and with luminance modulation response saturation accompanied by a phase advance between 10–20 Hz, characteristic of a contrast gain mechanism. This indicates a very similar retinal organization to Old-World monkeys. Cone-specific opsin expression in the presence of a locus control region for each opsin may call into question the hypothesis that this region exclusively controls opsin expression.     

Diurnality and cone photopigment polymorphism in strepsirrhines: examination of linkage in Lemur catta

Trichromatic color vision is routine among catarrhine primates, but occurs only as a variant form of color vision in some individuals in most platyrrhine genera. This arises from a fundamental difference in the organization of X-chromosome cone opsin genes in these two lineages: catarrhines have two opsin genes specifying middle- and long-wavelength-sensitive cone pigments, while platyrrhines have only a single gene. Some female platyrrhine monkeys achieve trichromacy because of a species polymorphism that allows the possibility of different opsin gene alleles on the two X-chromosomes. Recently, a similar opsin gene polymorphism was detected in some diurnal strepsirrhines, while at the same time appearing to be absent in any nocturnal genera. The aim of this study was to assess whether cone pigment polymorphism is inevitably linked to diurnality in strepsirrhines. Cone photopigments were measured in a species usually classified as diurnal, the ring-tailed lemur (Lemur catta), using electroretinogram flicker photometry, a noninvasive electrophysiological procedure. Each of 12 animals studied was found to have the same middle-wavelength cone pigment, with peak sensitivity at about 547 nm. In conjunction with earlier results, this implies that cone pigment polymorphism is unlikely to exist in this species and that, accordingly, such variation is not a consistently predictable feature of vision in diurnal strepsirrhines.     

Color vision diversity and significance in primates inferred from genetic and field studies

Color provides a reliable cue for object detection and identification during various behaviors such as foraging, mate choice, predator avoidance and navigation. The total number of colors that a visual system can discriminate is largely dependent on the number of different spectral types of cone opsins present in the retina and the spectral separations among them. Thus, opsins provide an excellent model system to study evolutionary interconnections at the genetic, phenotypic and behavioral levels. Primates have evolved a unique ability for three-dimensional color vision (trichromacy) from the two-dimensional color vision (dichromacy) present in the majority of other mammals. This was accomplished via allelic differentiation (e.g. most New World monkeys) or gene duplication (e.g. Old World primates) of the middle to long-wavelength sensitive (M/LWS, or red–green) opsin gene. However, questions remain regarding the behavioral adaptations of primate trichromacy. Allelic differentiation of the M/LWS opsins results in extensive color vision variability in New World monkeys, where trichromats and dichromats are found in the same breeding population, enabling us to directly compare visual performances among different color vision phenotypes. Thus, New World monkeys can serve as an excellent model to understand and evaluate the adaptive significance of primate trichromacy in a behavioral context. I shall summarize recent findings on color vision evolution in primates and introduce our genetic and behavioral study of vision-behavior interrelationships in free-ranging sympatric capuchin and spider monkey populations in Costa Rica.     

Color Vision Variation as Evidenced by Hybrid L/M Opsin Genes in Wild Populations of Trichromatic Alouatta New World Monkeys

Platyrrhine (New World) monkeys possess highly polymorphic color vision owing to allelic variation of the single-locus L/M opsin gene on the X chromosome. Most species consist of female trichromats and female and male dichromats. Howlers (genus Alouatta) are an exception; they are considered to be routinely trichromatic with L and M opsin genes juxtaposed on the X chromosome, as seen in catarrhine primates (Old World monkeys, apes, and humans). Yet it is not known whether trichromacy is invariable in howlers. We examined L/M opsin variation in wild howler populations in Costa Rica and Nicaragua (Alouatta palliata) and Belize (A. pigra), using fecal DNA. We surveyed exon 5 sequences (containing the diagnostic 277th and 285th residues for λ_max) for 8 and 18 X chromosomes from Alouatta palliata and A. pigra, respectively. The wavelengths of maximal absorption (λ_max) of the reconstituted L and M opsin photopigments were 564 nm and 532 nm, respectively, in both species. We found one M–L hybrid sequence with a recombinant 277/285 haplotype in Alouatta palliata and two L–M hybrid sequences in A. pigra. The λ_max values of the reconstituted hybrid photopigments were in the range of 546~554 nm, which should result in trichromat phenotypes comparable to those found in other New World monkey species. Our finding of color vision variation due to high frequencies of L/M hybrid opsin genes in howlers challenges the current view that howlers are routine and uniform trichromats. These results deepen our understanding of the evolutionary significance of color vision polymorphisms and routine trichromacy and emphasize the need for further assessment of opsin gene variation as well as behavioral differences among subtypes of trichromacy.     

What does it mean to be wild? Assessing human influence on the environments of nonhuman primate specimens in museum collections

ObjectivesNatural history collections are often thought to represent environments in a pristine natural state—free from human intervention—the so‐called “wild.” In this study, we aim to assess the level of human influence represented by natural history collections of wild‐collected primates over 120 years at the Smithsonian Institution''s National Museum of Natural History (NMNH).Materials and MethodsOur sample consisted of 875 catarrhine primate specimens in NMNH collections, representing 13 genera collected in 39 countries from 1882 to 2004. Using archival and accession information we determined the approximate locations from which specimens were collected. We then plotted location coordinates onto publicly available anthrome maps created by Ellis et al. (Global Ecology and Biogeography, 2010, 19, 589), which delineate terrestrial biomes of human population density and land use worldwide since the 1700s.ResultsWe found that among primates collected from their native ranges, 92% were from an environment that had some level of human impact, suggesting that the majority of presumed wild‐collected primate specimens lived in an environment influenced by humans during their lifetimes.DiscussionThe degree to which human‐modified environments may have impacted the lives of primates currently held in museum collections has been historically ignored, implicating unforeseen consequences for collection‐based research. While unique effects related to commensalism with humans remain understudied, effects currently attributed to natural phenomena may, in fact, be related to anthropogenic pressures on unmanaged populations of primates.     

Ultraviolet components offer minimal contrast enhancement to an aposematic signal

Aposematic and sexual signals are often characterized by bright, highly contrasting colors. Many species can see colors beyond the human visible spectrum, and ultraviolet (UV) reflection has been found to play an important role in communication and sexual selection. However, the role of UV in aposematic signals is poorly explored. Poison frogs frequently produce high‐contrast signals that have been linked to both aposematism and intraspecific communication. Yet despite considerable efforts studying interspecific and intraspecific diversity in color, poison frogs are not known to perceive UV, and UV reflection of the integument has not been described. We report UV‐reflective spots in a population of Oophaga sylvatica and quantify the effect of UV on visual contrast with models of avian vision. We found that the frogs are highly contrasting, but UV had a minimal effect on signal saliency. These data highlight the importance of considering UV reflectance within aposematic signals, but that UV should not necessarily be regarded as an independent signal.     

Opsin Genes and Visual Ecology in a Nocturnal Folivorous Lemur

Primate color vision has traditionally been examined in the context of diurnal activity, but recent genetic and ecological studies suggest that color vision plays a role in nocturnal primate behavior and ecology as well. In this study, we united molecular analyses of cone visual pigment (opsin) genes with visual modeling analyses of food items to explore the evolution of color vision in the folivorous woolly lemur (genus Avahi). Previous studies have shown that leaf quality, e.g., protein content, leaf toughness, and protein/toughness ratio, is significantly correlated with green-red and blue-yellow chromatic differences, suggesting a potential role of color in leaf discrimination in Avahi, and, consequently, a potential adaptive advantage to color vision in this taxon. Phylogenetic selection tests determined that the strength of selection on the SWS1 opsin gene to retain blue-sensitive SWS cones did not significantly differ in Avahi compared to day-active primates. Genotyping of the M/LWS opsin gene in 60 individuals from nine species found that the 558-nm-sensitive (red-sensitive) allele is conserved across all Avahi. Finally, we measured spectral reflectance from five species of young leaves consumed by Avahi and background foliage in Ranomafana National Park and modeled performance of possible S and M/L pigment pairs for detecting these food items under different nocturnal illuminations (e.g. twilight, moonlight). We found that the observed cone pigment pair in Avahi was optimally tuned for color-based detection of young green leaves in all nocturnal light environments, suggesting a potential adaptive role of nocturnal color vision in selection for dichromacy in this genus.     

Y-chromosomal red-green opsin genes of nocturnal New World monkey

The X-chromosomal locality of the red-green-sensitive opsin genes has been the norm for all mammals and is essential for color vision of higher primates. Owl monkeys (Aotus), a genus of New World monkeys, are the only nocturnal higher primates and are severely color-blind. We demonstrate that the owl monkeys possess extra red-green opsin genes on the Y-chromosome. The Y-linked opsin genes were found to be extremely varied, in one male appearing to be a functional gene and in other males to be multicopy pseudogenes. These Y-linked opsin genes should offer a rare opportunity to study the evolutionary fate of genes translocated to the Y chromosome.     

Signatures of functional constraint at aye-aye opsin genes: the potential of adaptive color vision in a nocturnal primate

While color vision perception is thought to be adaptively correlated with foraging efficiency for diurnal mammals, those that forage exclusively at night may not need color vision nor have the capacity for it. Indeed, although the basic condition for mammals is dichromacy, diverse nocturnal mammals have only monochromatic vision, resulting from functional loss of the short-wavelength sensitive opsin gene. However, many nocturnal primates maintain intact two opsin genes and thus have dichromatic capacity. The evolutionary significance of this surprising observation has not yet been elucidated. We used a molecular population genetics approach to test evolutionary hypotheses for the two intact opsin genes of the fully nocturnal aye-aye (Daubentonia madagascariensis), a highly unusual and endangered Madagascar primate. No evidence of gene degradation in either opsin gene was observed for any of 8 aye-aye individuals examined. Furthermore, levels of nucleotide diversity for opsin gene functional sites were lower than those for 15 neutrally evolving intergenic regions (>25 kb in total), which is consistent with a history of purifying selection on aye-aye opsin genes. The most likely explanation for these findings is that dichromacy is advantageous for aye-ayes despite their nocturnal activity pattern. We speculate that dichromatic nocturnal primates may be able to perceive color while foraging under moonlight conditions, and suggest that behavioral and ecological comparisons among dichromatic and monochromatic nocturnal primates will help to elucidate the specific activities for which color vision perception is advantageous.     

Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates

Olfactory receptor (OR) genes constitute the molecular basis for the sense of smell and are encoded by the largest gene family in mammalian genomes. Previous studies suggested that the proportion of pseudogenes in the OR gene family is significantly larger in humans than in other apes and significantly larger in apes than in the mouse. To investigate the process of degeneration of the olfactory repertoire in primates, we estimated the proportion of OR pseudogenes in 19 primate species by surveying randomly chosen subsets of 100 OR genes from each species. We find that apes, Old World monkeys and one New World monkey, the howler monkey, have a significantly higher proportion of OR pseudogenes than do other New World monkeys or the lemur (a prosimian). Strikingly, the howler monkey is also the only New World monkey to possess full trichromatic vision, along with Old World monkeys and apes. Our findings suggest that the deterioration of the olfactory repertoire occurred concomitant with the acquisition of full trichromatic color vision in primates.     

Color vision of ancestral organisms of higher primates

The color vision of mammals is controlled by photosensitive proteins called opsins. Most mammals have dichromatic color vision, but hominoids and Old World (OW) monkeys enjoy trichromatic vision, having the blue-, green-, and red-sensitive opsin genes. Most New World (NW) monkeys are either dichromatic or trichromatic, depending on the sex and genotype. Trichromacy in higher primates is believed to have evolved to facilitate the detection of yellow and red fruits against dappled foliage, but the process of evolutionary change from dichromacy to trichromacy is not well understood. Using the parsimony and the newly developed Bayesian methods, we inferred the amino acid sequences of opsins of ancestral organisms of higher primates. The results suggest that the ancestors of OW and NW monkeys lacked the green gene and that the green gene later evolved from the red gene. The fact that the red/green opsin gene has survived the long nocturnal stage of mammalian evolution and that it is under strong purifying selection in organisms that live in dark environments suggests that this gene has another important function in addition to color vision, probably the control of circadian rhythms.      

Intraspecific interactions in a high‐density leopard population

Although less studied than interspecific interactions, interactions among members of the same species can influence space use and temporal activity. Using techniques commonly applied to the analysis of interspecific interactions—multispecies occupancy modeling and the analysis of temporal activity patterns—we studied intraspecific interactions within a high‐density population of Persian leopards (Panthera pardus saxicolor) in Tandoureh National Park, northeastern Iran. Using camera‐trap data, we investigated spatiotemporal interactions between male leopards, lone female leopards, and families (cubs/females with cubs). While we hypothesized that male and female leopards would display different temporal activity patterns, we did not predict spatial avoidance between these groups. We also predicted that leopard families would exhibit spatiotemporal avoidance from male leopards due to the risk of infanticide. Contrary to our expectations, we did not find any evidence for spatial or temporal avoidance between leopard families and adult male leopards. Male and lone female leopards exhibited positive pairwise co‐occurrence, consistent with reports of high overlap between male and female leopard home ranges. While a high level of overlap in temporal activity patterns was found between males/lone females and males/families, there was evidence for variation in the proportion of time each leopard group was active in particular periods of the diel cycle. Male leopards showed cathemeral activity, while lone females and families were more active during daylight hours. The application of these techniques to interactions within a species has improved understanding of the ecology and behavior of this endangered solitary carnivore.     

Mutational changes in S-cone opsin genes common to both nocturnal and cathemeral Aotus monkeys

Aotus is a platyrrhine primate that has been classically considered to be nocturnal. Earlier research revealed that this animal lacks a color vision capacity because, unlike all other platyrrhine monkeys, Aotus has a defect in the opsin gene that is required to produce short-wavelength sensitive (S) cone photopigment. Consequently, Aotus retains only a single type of cone photopigment. Other mammals have since been found to show similar losses and it has often been speculated that such change is in some fashion tied to nocturnality. Although most species of Aotus are indeed nocturnal, recent observations show that Aotus azarai, an owl monkey species native to portions of Argentina and Paraguay, displays a cathemeral activity pattern being active during daylight hours as frequently as during nighttime hours. We have sequenced portions of the S-cone opsin gene in A. azarai and Aotus nancymaae, the latter a typically nocturnal species. The S-cone opsin genes in both species contain the same fatal defects earlier detected for Aotus trivirgatus. On the basis of the phylogenetic relationships of these three species these results imply that Aotus must have lost a capacity for color vision early in its history and they also suggest that the absence of color vision is not compulsively linked to a nocturnal lifestyle.