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.
According to the sensory drive model, variation in visual properties can lead to diverse female preferences, which in turn results in a range of male nuptial colors by way of sexual selection. ...However, the cause of variation in visual properties and the mechanism by which variation drives female response to visual signals remain unclear. Here, we demonstrate that both differences in the long-wavelength–sensitive 1 (LWS-1) opsin genotype and the light environment during rearing lead to variation in opsin gene expression. Opsin expression variation affects the visual sensitivity threshold to long wavelengths of light. Moreover, a behavioral assay using digitally modified video images showed that the expression of multiple opsin genes is positively correlated with the female responsiveness to images of males with luminous orange spots. The findings suggest that genetic polymorphisms and light environment in habitats induce variations in opsin gene expression levels. The variations may facilitate variations in visual sensitivity and female responsiveness to male body colors within and among populations.
The senses play critical roles in helping animals evaluate foods, including fruits that can change both in colour and scent during ripening to attract frugivores. Although numerous studies have ...assessed the impact of colour on fruit selection, comparatively little is known about fruit scent and how olfactory and visual data are integrated during foraging. We combine 25 months of behavioural data on 75 wild, white-faced capuchins (Cebus imitator) with measurements of fruit colours and scents from 18 dietary plant species. We show that frequency of fruit-directed olfactory behaviour is positively correlated with increases in the volume of fruit odours produced during ripening. Monkeys with red-green colour blindness sniffed fruits more often, indicating that increased reliance on olfaction is a behavioural strategy that mitigates decreased capacity to detect red-green colour contrast. These results demonstrate a complex interaction among fruit traits, sensory capacities and foraging strategies, which help explain variation in primate behaviour.
Proper functioning of sensory systems requires the generation of appropriate numbers and proportions of neuronal subtypes that encode distinct information. Perception of color relies on signals from ...multiple cone photoreceptor types. In cone-dominated retinas, each cone expresses a single opsin type with peak sensitivity to UV, long (L) (red), medium (M) (green), or short (S) (blue) wavelengths. The modes of cell division generating distinct cone types are unknown. We report here a mechanism whereby zebrafish cone photoreceptors of the same type are produced by symmetric division of dedicated precursors. Transgenic fish in which the thyroid hormone receptor β2 (trβ2) promoter drives fluorescent protein expression before L-cone precursors themselves are produced permitted tracking of their division in vivo. Every L cone in a local region resulted from the terminal division of an L-cone precursor, suggesting that such divisions contribute significantly to L-cone production. Analysis of the fate of isolated pairs of cones and time-lapse observations suggest that other cone types can also arise by symmetric terminal divisions. Such divisions of dedicated precursors may help to rapidly attain the final numbers and proportions of cone types (L > M, UV > S) in zebrafish larvae. Loss-and gain-of-function experiments show that L-opsin expression requires trftë activity before cone differentiation. Ectopic expression of trβ2 after cone differentiation produces cones with mixed opsins. Temporal differences in the onset of trβ2 expression could explain why some species have mixed, and others have pure, cone types.
Abstract
Gene duplication of green (RH2) opsin genes and their spectral differentiation are well documented in many teleost fish. However, their evolutionary divergence or conservation patterns among ...phylogenetically close but ecologically diverse species is not well explored. Medaka fish (genus Oryzias) are broadly distributed in fresh and brackish waters of Asia, with many species being laboratory-housed and feasible for genetic studies. We previously showed that a Japan strain (HNI) of medaka (Oryzias latipes) possessed three RH2 opsin genes (RH2-A, RH2-B, and RH2-C) encoding spectrally divergent photopigments. Here, we examined the three RH2 opsin genes from six Oryzias species representing three species groups: the latipes, the celebensis, and the javanicus. Photopigment reconstitution revealed that the peak absorption spectra (λmax) of RH2-A were divergent among the species (447–469 nm), whereas those of RH2-B and RH2-C were conservative (516–519 and 486–493 nm, respectively). For the RH2-A opsins, the largest spectral shift was detected in the phylogenetic branch leading to the latipes group. A single amino acid replacement T94C explained most of the spectral shift. For RH2-B and -C opsins, we detected tracts of gene conversion between the two genes homogenizing them. Nevertheless, several amino acid differences were maintained. We showed that the spectral difference between the two opsins was attributed to largely the E/Q amino acid difference at the site 122 and to several sites with individually small spectral effects. These results depict dynamism of spectral divergence of orthologous and paralogous green opsin genes in phylogenetically close but ecologically diverse species exemplified by medaka.
Endocrine regulation of multichromatic color vision Mackin, Robert D.; Frey, Ruth A.; Gutierrez, Carmina ...
Proceedings of the National Academy of Sciences,
08/2019, Letnik:
116, Številka:
34
Journal Article
Recenzirano
Odprti dostop
Vertebrate color vision requires spectrally selective opsin-based pigments, expressed in distinct cone photoreceptor populations. In primates and in fish, spectrally divergent opsin genes may reside ...in head-to-tail tandem arrays. Mechanisms underlying differential expression from such arrays have not been fully elucidated. Regulation of human red (LWS) vs. green (MWS) opsins is considered a stochastic event, whereby upstream enhancers associate randomly with promoters of the proximal or distal gene, and one of these associations becomes permanent. We demonstrate that, distinct from this stochastic model, the endocrine signal thyroid hormone (TH) regulates differential expression of the orthologous zebrafish lws1/lws2 array, and of the tandemly quadruplicated rh2-1/rh2-2/rh2-3/rh2-4 array. TH treatment caused dramatic, dose-dependent increases in abundance of lws1, the proximal member of the lws array, and reduced lws2. Fluorescent lws reporters permitted direct visualization of individual cones switching expression from lws2 to lws1. Athyroidism increased lws2 and reduced lws1, except within a small ventral domain of lws1 that was likely sustained by retinoic acid signaling. Changes in lws abundance and distribution in athyroid zebrafish were rescued by TH, demonstrating plasticity of cone phenotype in response to this signal. TH manipulations also regulated the rh2 array, with athyroidism reducing abundance of distal members. Interestingly, the opsins encoded by the proximal lws gene and distal rh2 genes are sensitive to longer wavelengths than other members of their respective arrays; therefore, endogenous TH acts upon each opsin array to shift overall spectral sensitivity toward longer wavelengths, underlying coordinated changes in visual system function during development and growth.
The olfactory receptor (OR) gene family is comprised of hundreds of intact and disrupted genes in humans. The compositions and copy number variation (CNV) of disrupted and intact OR genes among ...individuals is expected to cause variation in olfactory perception. However, little is known about OR genetic variation in many human populations. In this study, we used targeted capture enrichment and massive parallel short-read sequencing methods to examine genetic variation of OR genes, as well as of neutral genome regions as references, for 69 anonymized unrelated Japanese individuals. The capture probes were designed for 398 intact OR genes in the human reference genome hg38, and 85 neutral references. Probes were also designed for four unannotated and 99 ‘nearly-intact’ (hg38-pseudo) OR genes in hg38 and 53 chimpanzee OR genes in the Pantro3.0 genome database with no orthologs in hg38. All the hg38 OR genes and one Pantro 3.0 OR gene were retrieved. The mean sequencing depth was significantly higher than that of the 1000 Genomes Project. A total of 30 OR genes from hg38-intact and hg38-pseudo categories were newly found to be segregating pseudogenes. One hg38-pseudo OR gene was intact in all individuals. CNV was detected in 63 OR genes. Tajima’s D analysis for OR genes and neutral references was consistent with balancing selection to maintain allelic differences in intact OR genes. These results demonstrate that the targeted capture by probes with diversity-oriented design is far more effective than a whole-genome approach to retrieve OR genes and achieve high-depth sequencing and thus to reveal polymorphisms for the OR multigene family. The composition of OR genes in the human reference genome hg38 does not necessarily represent those in many humans, implying higher perceptual variation than previously thought. The current study inspires further investigation with a similar approach at a global scale.
In environments with multiple predators, vulnerabilities associated with the spatial positions of group-living prey are non-uniform and depend on the hunting styles of the predators. Theoretically, ...coursing predators follow their prey over long distances and attack open areas, exposing individuals at the edge of the group to predation risk more than those at the center (marginal predation). In contrast, ambush predators lurk unnoticed by their prey and appear randomly anywhere in the group; therefore, isolated individuals in the group would be more vulnerable to predators. These positions of vulnerability to predation are expected to be taken by larger-bodied males. Moreover, dominant males presumably occupy the center of the safe group. However, identifying individuals at higher predation risk requires both simultaneous recording of predator location and direct observation of predation events; empirical observations leave ambiguity as to who is at risk. Instead, several theoretical methods (predation risk proxies) have been proposed to assess predation risk: (1) the size of the individual 'unlimited domain of danger' based on Voronoi tessellation, (2) the size of the 'limited domain of danger' based on predator detection distance, (3) peripheral/center position in the group (minimum convex polygon), (4) the number and direction of others in the vicinity (surroundedness), and (5) dyadic distances. We explored the age-sex distribution of individuals in at-risk positions within a wild baboon group facing predation risk from leopards, lions, and hyenas, using Global Positioning System collars. Our analysis of the location data from 26 baboons revealed that adult males were consistently isolated at the edge of the group in all predation risk proxies. Empirical evidence from previous studies indicates that adult male baboons are the most frequently preyed upon, and our results highlights the importance of spatial positioning in this.
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