Gene conversion and natural selection in the evolution of X-linked color vision genes in higher primates

During higher primate evolution, gene conversion seems to have occurred often between the red and green photo-pigment genes, which are tandemly linked on the X chromosome. To understand this phenomenon better, intron 4 sequences of the red and green pigment genes of a male human (an Asian Indian), a male chimpanzee, and a male baboon were amplified by PCR and sequenced. The data show that the intron 4 sequences between the two genes have been strongly or completely homogenized in the three species studied. Apparently recent gene conversion events have occurred in introns 4 of the red and green pigment genes in humans and chimpanzees. Two or more conversion events may have occurred at different times in introns 4 of the two pigment genes in baboons. The divergence between the two genes is significantly lower in intron 4 than in exons 4 and 5 in each species, contrary to the usual situation that introns evolve faster than exons. It is most likely that strong natural selection for maintaining the distinct functions of exons 4 and 5 of the red and green pigment genes has acted against sequence homogenization of these exons.      

Historical contingency in the evolution of primate color vision

Primates are unique among eutherian mammals for possessing three types of retinal cone. Curiously, catarrhines, platyrrhines, and strepsirhines share this anatomy to different extents, and no hypothesis has hitherto accounted for this variability. Here we propose that the historical biogeography of figs and arborescent palms accounts for the global variation in primate color vision. Specifically, we suggest that primates invaded Paleogene forests characterized by figs and palms, the fruits of which played a keystone function. Primates not only relied on such resources, but also provided high-quality seed dispersal. In turn, figs and palms lost or simply did not evolve conspicuous coloration, as this conferred little advantage for attracting mammals. We suggest that the abundance and coloration of figs and palms offered a selective advantage to foraging groups with mixed capabilities for chromatic distinction. Climatic cooling at the end of the Eocene and into the Neogene resulted in widespread regional extinction or decimation of palms and (probably) figs. In regions where figs and palms became scarce, we suggest primates evolved routine trichromatic vision in order to exploit proteinaceous young leaves as a replacement resource. A survey of the hue and biogeography of extant figs and palms provides some empirical support. Where these resources are infrequent, primates are routinely trichromatic and consume young leaves during seasonal periods of fruit dearth. These results imply a link between the differential evolution of primate color vision and climatic changes during the Eocene-Oligocene transition.     

Molecular evolution of bat color vision genes

The two suborders of bats, Megachiroptera (megabats) and Microchiroptera(microbats), use different sensory modalities for perceivingtheir environment. Megabats are crepuscular and rely on a well-developedeyes and visual pathway, whereas microbats occupy a nocturnalniche and use acoustic orientation or echolocation more thanvision as the major means of perceiving their environment. Inview of the differences associated with their sensory systems,we decided to investigate the function and evolution of colorvision (opsin genes) in these two suborders of bats. The middle/longwavelength (M/L) and short wavelength (S) opsin genes were sequencedfrom two frugivorous species of megabats, Haplonycteris fischeriand Pteropus dasymallus formosus, and one insectivorous speciesof microbat, Myotis velifer. Contrary to the situation in primates,where many nocturnal species have lost the functional S opsingene, both crepuscular and strictly nocturnal species of batsthat we examined have functional M/L and S opsin genes. Surprisingly,the S opsin in these bats may be sensitive to UV light, whichis relatively more abundant at dawn and at dusk. The M/L opsinin these bats appears to be the L type, which is sensitive tored and may be helpful for identifying fruits among leaves orfor other purposes. Most interestingly, H. fischeri has a recentduplication of the M/L opsin gene, representing to date theonly known case of opsin gene duplication in non-primate mammals.Some of these observations are unexpected and may provide insightsinto the effect of nocturnal life on the evolution of opsingenes in mammals and the evolution of the life history traitsof bats in general.     

Seeing red: behavioral evidence of trichromatic color vision in strepsirrhine primates

Among primates, catarrhines (Old World monkeys and apes) andcertain platyrrhines (New World monkeys) possess trichromaticcolor vision, which might confer important evolutionary advantages,particularly during foraging. Recently, a polymorphism has beenshown to shift the spectral sensitivity of the X-linked opsinprotein in certain strepsirrhines (e.g., Malagasy lemurs); however,its behavioral significance remains unknown. We assign genotypesat the X-linked variant to 45 lemurs, representing 4 species,and test if the genetic capacity for trichromacy impacts foragingperformance, particularly under green camouflage conditionsin which red detection can be advantageous. We confirm polymorphismat the critical site in sifakas and ruffed lemurs and fail tofind this polymorphism in collared lemurs and ring-tailed lemurs.We show that this polymorphism may be linked to "behavioraltrichromacy" in heterozygous ruffed lemurs but find no comparableevidence in a single heterozygous sifaka. Despite their putativedichromatic vision, female collared lemurs were surprisinglyefficient at retrieving both red and green food items undercamouflage conditions. Thus, species-specific feeding ecologiesmay be as important as trichromacy in influencing foraging behavior.Although the lemur opsin polymorphism produced measurable behavioraleffects in at least one species, the ruffed lemur, these effectswere modest, consistent with the modest shift in spectral sensitivity.Additionally, the magnitude of these effects varied across individualsof the same genotype, emphasizing the need for combined geneticand behavioral studies of trichromatic vision. We conclude thattrichromacy may be only one of several routes toward increasedforaging efficiency in visually complex environments.     

Molecular evolution of color vision of zebra finch

We have isolated and sequenced the RH1(Tg), RH2(Tg), SWS2(Tg), and LWS(Tg) opsin cDNAs from zebra finch retinas. Upon binding to 11-cis-retinal, these opsins regenerate the corresponding photosensitive molecules, visual pigments. The absorption spectra of visual pigments have a broad bell shape, with the peak being called lambda(max). Previously, SWS1(Tg) opsin cDNA was isolated from zebra finch retinal RNA, expressed in cultured COS1 cells, reconstituted with 11-cis-retinal, and the lambda(max) of the resulting visual pigment was shown to be 359nm. Here, the lambda(max) values of the RH1(Tg), RH2(Tg), SWS2(Tg), and LWS(Tg) pigments are determined to be 501, 505, 440, and 560nm, respectively. Molecular evolutionary analyses suggest that specific amino acid replacements in the SWS1 and SWS2 pigments, resulting from accelerated evolution, must have been responsible for their functional divergences among the avian pigments.     

Intronic gene conversion in the evolution of human X-linked color vision genes

Human red and green visual pigment genes are X-linked duplicate genes. To study their evolutionary history, introns 2 and 4 (1,987 and 1,552 bp, respectively) of human red and green pigment genes were sequenced. Surprisingly, we found that intron 4 sequences of these two genes are identical and that the intron 2 sequences differ by only 0.3%. The low divergences are unexpected because the duplication event producing the two genes is believed to have occurred before the separation of the human and Old World monkey (OWM) lineages. Indeed, the divergences in the two introns are significantly lower than both the synonymous divergence (3.2% +/- 1.1%) and the nonsynonymous divergence (2.0% +/- 0.5%) in the coding sequences (exons 1-6). A comparison of partial sequences of exons 4 and 5 of human and OWM red and green pigment genes supports the hypothesis that the gene duplication occurred before the human-OWM split. In conclusion, the high similarities in the two intron sequences might be due to very recent gene conversion, probably during evolution of the human lineage.      

Sexual selection and trichromatic color vision in primates: statistical support for the preexisting-bias hypothesis

The evolution of trichromatic color vision in primates may improve foraging performance as well as intraspecific communication; however, the context in which color vision initially evolved is unknown. We statistically examined the hypothesis that trichromatic color vision in primates represents a preexisting bias for the evolution of red coloration (pelage and/or skin) through sexual selection. Our analyses show that trichromatic color vision evolved before red pelage and red skin, as well as before gregarious mating systems that would promote sexual selection for visual traits and other forms of intraspecific communication via red traits. We also determined that both red pelage and red skin were more likely to evolve in the presence of color vision and mating systems that promote sexual selection. These results provide statistical support for the hypothesis that trichromatic color vision in primates evolved in a context other than intraspecific communication with red traits, most likely foraging performance, but, once evolved, represented a preexisting bias that promoted the evolution of red traits through sexual selection.     

Avian vision and the evolution of egg color mimicry in the common cuckoo

Coevolutionary arms races are a potent force in evolution, and brood parasite-host dynamics provide classical examples. Different host-races of the common cuckoo, Cuculus canorus, lay eggs in the nests of other species, leaving all parental care to hosts. Cuckoo eggs often (but not always) appear to match remarkably the color and pattern of host eggs, thus reducing detection by hosts. However, most studies of egg mimicry focus on human assessments or reflectance spectra, which fail to account for avian vision. Here, we use discrimination and tetrachromatic color space modeling of bird vision to quantify egg background and spot color mimicry in the common cuckoo and 11 of its principal hosts, and we relate this to egg rejection by different hosts. Egg background color and luminance are strongly mimicked by most cuckoo host-races, and mimicry is better when hosts show strong rejection. We introduce a novel measure of color mimicry-"color overlap"-and show that cuckoo and host background colors increasingly overlap in avian color space as hosts exhibit stronger rejection. Finally, cuckoos with better background color mimicry also have better pattern mimicry. Our findings reveal new information about egg mimicry that would be impossible to derive by the human eye.     

The evolution of monogamy in primates

The evolution of primate monogamy is described as an ordered sequence of choices by generalized, hypothetical females and males. Females first choose whether or not to associate with other females. Predators encourage gregariousness in diurnal primates; however, nocturnality or scarce and evenly distributed food supplies may enforce separation. A testable group size model based on food patch size is developed and qualitatively supported.If females choose solitude, males then choose either to defend a single female and invest in her offspring, or to compete with other males for access to several females, usually by defending a territory or establishing dominance over the home ranges of several females. The decision rests on the defensibility of females and on the availability of an effective form of male parental investment. Both of these factors are dependent on local female population density. A model is developed that assumes that territorial defense is the principal form of male parental investment, and it predicts that monogamy should occur at intermediate densities: at high densities, males should switch to defense of multiple females, and at low densities there is no investment value in male territorial defense. The model is shown to be only partly adequate. Variation in local population densities prevents the establishment of obligate monogamy through territoriality in small monkeys, since male territorial behavior is inconsistent over the long run. Here, carrying of offspring by males can succeed territoriality, providing an effective and reliable form of parental investment to maintain the pair bond in the face of population fluctuations and changes in group structure. This hypothesis is supported by the scarcity of obligate monogamy among the prosimians, which frequently do not carry their young.     

The molecular genetics and evolution of red and green color vision in vertebrates.

To better understand the evolution of red-green color vision in vertebrates, we inferred the amino acid sequences of the ancestral pigments of 11 selected visual pigments: the LWS pigments of cave fish (Astyanax fasciatus), frog (Xenopus laevis), chicken (Gallus gallus), chameleon (Anolis carolinensis), goat (Capra hircus), and human (Homo sapiens);and the MWS pigments of cave fish, gecko (Gekko gekko), mouse (Mus musculus), squirrel (Sciurus carolinensis), and human. We constructed these ancestral pigments by introducing the necessary mutations into contemporary pigments and evaluated their absorption spectra using an in vitro assay. The results show that the common ancestor of vertebrates and most other ancestors had LWS pigments. Multiple regression analyses of ancestral and contemporary MWS and LWS pigments show that single mutations S180A, H197Y, Y277F, T285A, A308S, and double mutations S180A/H197Y shift the lambda(max) of the pigments by -7, -28, -8, -15, -27, and 11 nm, respectively. It is most likely that this "five-sites" rule is the molecular basis of spectral tuning in the MWS and LWS pigments during vertebrate evolution.     

Trans-specific evolution of opsin alleles and the maintenance of trichromatic colour vision in Callitrichine primates

Many New World (NW) primates possess a remarkable polymorphism in an X-linked locus, which encodes for the visual pigments (opsins) used for colour vision. Females that are heterozygous for opsin alleles of different spectral sensitivity at this locus have trichromatic colour vision, whereas homozygous females and males are dichromatic, with poor colour discrimination in the red-green range. Here we describe an extensive survey of allelic variation in both exons and introns at this locus within and among species of the Callitrichines (marmosets and tamarins). All five genera of Callitrichines have the X-linked polymorphism, and only the three functional allelic classes described previously (with maximum wavelength sensitivities at about 543 nm, 556 nm and 563 nm) were found among the 16 species and 233 or more X-chromosomes sampled. In spite of the homogenizing effects of gene conversion, phylogenetic analyses provide direct evidence for trans-specific evolution of alleles over time periods of at least 5-6 million years, and up to 14 million years (estimated from independent phylogenies). These conclusions are supported by the distribution of insertions and deletions in introns. The maintenance of polymorphism over these time periods requires an adaptive explanation, which must involve a heterozygote advantage for trichromats. The lack of detection of alleles that are recombinant for spectral sensitivity suggests that such alleles are suboptimal. The two main hypotheses for the selective advantage of trichromacy in primates are frugivory for ripe fruits and folivory for young leaves. The latter can be discounted in Callitrichines, as they are not folivorous.     

The evolution of face processing in primates

The ability to recognize faces is an important socio-cognitive skill that is associated with a number of cognitive specializations in humans. While numerous studies have examined the presence of these specializations in non-human primates, species where face recognition would confer distinct advantages in social situations, results have been mixed. The majority of studies in chimpanzees support homologous face-processing mechanisms with humans, but results from monkey studies appear largely dependent on the type of testing methods used. Studies that employ passive viewing paradigms, like the visual paired comparison task, report evidence of similarities between monkeys and humans, but tasks that use more stringent, operant response tasks, like the matching-to-sample task, often report species differences. Moreover, the data suggest that monkeys may be less sensitive than chimpanzees and humans to the precise spacing of facial features, in addition to the surface-based cues reflected in those features, information that is critical for the representation of individual identity. The aim of this paper is to provide a comprehensive review of the available data from face-processing tasks in non-human primates with the goal of understanding the evolution of this complex cognitive skill.     

The molecular genetics of color vision and color blindness

Recent reports from several laboratories have changed our thinking about the molecular genetics of normal color vision and color blindness. The impact of these new findings can be best appreciated by examining them in the context of the historical development of color vision theory.     

Object-based vision and attention in primates

In forming a representation of a visible object, the brain must analyze the visual scene pre-attentively, select an object through active attention, and form representations of the multiple attributes of the selected object. During the past two years, progress has been made in understanding the neural underpinnings of these processes by means of single-neuron recording in monkeys.     

Different selective pressures shape the molecular evolution of color vision in chimpanzee and human populations

A population genetic analysis of the long-wavelength opsin (OPN1LW, "red") color vision gene in a global sample of 236 human nucleotide sequences had previously discovered nine amino acid replacement single nucleotide polymorphisms, which were found at high frequencies in both African and non-African populations and associated with an unusual haplotype diversity. Although this pattern of nucleotide diversity is consistent with balancing selection, it has been argued that a recombination "hot spot" or gene conversion within and between X-linked color vision genes alone may explain these patterns. The current analysis investigates a closely related primate with trichromatism to determine whether color vision gene amino acid polymorphism and signatures of adaptive evolution are characteristic of humans alone. Our population sample of 56 chimpanzee (Pan troglodytes) OPN1LW sequences shows three singleton amino acid polymorphisms and no unusual recombination or linkage disequilibrium patterns across the approximately 5.5-kb region analyzed. Our comparative population genetic approach shows that the patterns of OPN1LW variation in humans and chimpanzees are consistent with positive and purifying selection within the two lineages, respectively. Although the complex role of color vision has been greatly documented in primate evolution in general, it is surprising that trichromatism has followed very different selective trajectories even between humans and our closest relatives.     

The evolution of social philopatry in female primates

The transition from solitary life to sociality is considered one of the major transitions in evolution. In primates, this transition is currently not well understood. Traditional verbal models appear insufficient to unravel the complex interplay of environmental and demographic factors involved in the evolution of primate sociality, and recent phylogenetic reconstructions have produced conflicting results. We therefore analyze a theoretical model for the evolution of female social philopatry that sheds new light on the question why most primates live in groups. In individual-based simulations, we study the evolution of dispersal strategies of both resident females and their offspring. The model reveals that social philopatry can evolve through kin selection, even if retention of offspring is costly in terms of within-group resource competition and provides no direct benefits. Our model supports the role of predator avoidance as a selective pressure for group-living in primates, but it also suggests that a second benefit of group-living, communal resource defense, might be required to trigger the evolution of sizable groups. Lastly, our model reveals that seemingly small differences in demographic parameters can have profound effects on primate social evolution.     

The relative rate of DNA evolution in primates

In 73 relative-rate tests involving the sequences of 17 genes between humans and six nonhuman primate taxa, there is only one significant (P less than 0.01) difference in evolutionary rate--i.e., that between human and Old World-monkey psi eta-globin genes. No evolutionary rate difference between humans and Old World monkeys is evident from analysis of 18 other genes with a total length of 6 kb. This and the comparison, between humans and other primate taxa, of new extended psi eta-globin sequences suggest that earlier observations of evolutionary-rate differences between humans and other primates were based on differences that are peculiar to psi eta-globin and that are not representative of the whole genome, which appears to be evolving at a stochastically uniform rate. This is supported by whole-genome single-copy DNA and mitochondrial DNA comparisons, neither of which shows any evidence of evolutionary-rate variation among primate taxa. Uniformity in the evolutionary rate of the DNA of primate and other mammalian taxa is inconsistent with current mammalian fossil-record interpretation. Either there has been a general slowing down in rate across lineages or the fossil record has been misinterpreted.