Evolution and selection of trichromatic vision in primates

Surridge, Alison K.; Osorio, Daniel; Mundy, Nicholas I.

doi:10.1016/s0169-5347(03)00012-0

Cited by 280 publications

(217 citation statements)

References 65 publications

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“…This vision-based signaling mechanism may have in part replaced the chemical-based pheromone signaling in the former group of organisms (43), because sexual swelling can be perceived from a distance, whereas pheromone perception is probably through physical contact (44). It is interesting to relate this observation to the duplication of the X-chromosome-linked red͞green-sensitive opsin gene that also occurred in the common ancestors of OW monkeys and hominoids after they were separated from NW monkeys, although a more precise date of the duplication has yet to be obtained (45,46). The gene duplication and subsequent functional divergence led to the emergence of a trichromatic color vision (with the blue, green, and red opsins) in both sexes, in contrast to the situation before the duplication when only females may have had trichromacy due to the existence of functionally polymorphic alleles at the red͞green opsin locus (46,47).…”

Section: Resultsmentioning

confidence: 99%

Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates

Zhang

Webb

2003

Proc. Natl. Acad. Sci. U.S.A.

236

209

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Pheromones are water-soluble chemicals released and sensed by individuals of the same species to elicit social and reproductive behaviors or physiological changes; they are perceived primarily by the vomeronasal organ (VNO) in terrestrial vertebrates. Humans and some related primates possess only vestigial VNOs and have no or significantly reduced ability to detect pheromones, a phenomenon not well understood at the molecular level. Here we show that genes encoding the TRP2 ion channel and V1R pheromone receptors, two components of the vomeronasal pheromone signal transduction pathway, have been impaired and removed from functional constraints since shortly before the separation of hominoids and Old World monkeys Ϸ23 million years ago, and that the random inactivation of pheromone receptor genes is an ongoing process even in present-day humans. The phylogenetic distribution of vomeronasal pheromone insensitivity is concordant with those of conspicuous female sexual swelling and male trichromatic color vision, suggesting that a vision-based signaling-sensory mechanism may have in part replaced the VNO-mediated chemical-based system in the social͞reproductive activities of hominoids and Old World monkeys (catarrhines). P heromones are water-soluble chemicals used in intraspecific communications to elicit social and reproductive behaviors or physiological changes such as male-male aggression, onset of puberty, estrus, and induction of mating. Pheromones are perceived primarily by the vomeronasal organ (VNO), which is at the base of the nasal cavity and separated from the main olfactory epithelium that senses thousands of volatile odorants (1). It has been known for decades that some primate species, including humans, do not possess functional VNOs, and these organisms lack vomeronasal chemoreception to pheromones (1-3). This insensitivity has likely had important impacts on the sexual and social behaviors of many primates. On the other hand, behavioral changes may have also altered natural selection on vomeronasal chemoreception. It is therefore of interest to find when the vomeronasal pheromone insensitivity occurred in evolution, how it occurred, and why it occurred.Vomeronasal pheromone perception begins by the binding of pheromones to pheromone receptors located on the cell membrane of sensory neurons of the VNO, which triggers a signal transduction pathway that ultimately leads to the activation of the hypothalamus. Several components in the pathway have been identified, including GTP-binding proteins, phospholipase C, inositol 1,4,5-trisphosphate (IP3), and an ion channel of the transient receptor potential family named TRP2 (also known as TRPC2) (4). However, among members of this pathway, only TRP2 (5) and pheromone receptors of the V1R and V2R families (6-9) are unique to pheromone transduction and are not known to be used in other physiological processes. Disruption of either of these two components in mice hampers pheromone perception and causes dramatic changes in sexual and social behaviors (10-12). Th...

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Section: Resultsmentioning

confidence: 99%

Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates

Zhang

Webb

2003

Proc. Natl. Acad. Sci. U.S.A.

236

209

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“…Trichromacy allowed primates to occupy new niches, moving from a nocturnal to a diurnal lifestyle and also to a frugivorous diet and the selection of food based on cues such as colour [81].…”

Section: Trichromacy Social Complexity and Pheromonesmentioning

confidence: 99%

The evolution of pheromonal communication

Swaney

Keverne

2009

Behavioural Brain Research

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Small-brained rodents have been the principle focus for pheromonal research and have provided comprehensive insights into the chemosensory mechanisms that underpin pheromonal communication and the hugely important roles that pheromones play in behavioural regulation. However, pheromonal communication does not start or end with the mouse and the rat, and work in amphibians reveals much about the likely evolutionary origins of the chemosensory systems that mediate pheromonal effects. The dual olfactory organs (the main olfactory epithelium and the vomeronasal organ), their receptors and their separate projection pathways appear to have ancient evolutionary origins, appearing in the aquatic ancestors of all tetrapods during the Devonian period and so pre-dating the transition to land. While the vomeronasal organ has long been considered an exclusively pheromonal organ, accumulating evidence indicates that it is not the sole channel for the transduction of pheromonal information and that both olfactory systems have been co-opted for the detection of different pheromone signals over the course of evolution. This has also led to great diversity in the vomeronasal and olfactory receptor families, with enormous levels of gene diversity and inactivation of genes in different species. Finally, the evolution of trichromacy as well as huge increases in social complexity have minimised the role of pheromones in the lives of primates, leading to the total inactivation of the vomeronasal system in catarrhine primates while the brain increased in size and behaviour became emancipated from hormonal regulation.

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“…Primates are unique among mammals in that most have trichromatic color vision. It has been hypothesized that being able to detect red fruits against a green background is the reason that trichromatic color vision evolved in primates (reviewed by Surridge et al 2003). When scientists consider which hues individuals with trichromatic vision can see, they have argued that trichromatic phenotypes are better suited than dichromats at discriminating ripe fruit hues (red, orange, and yellow; Regan et al 2001; although see Riba-Hernandez et al 2004) and young red leaves (Lucas et al 1998) from nonripe fruits and leaf background.…”

Section: In What Context Did Trichromatic Color Vision Evolve In Primmentioning

confidence: 99%

“…Several studies have noted that primates use red colors for intraspecific signaling (reviewed by Surridge et al 2003, Fig. 2).…”

Section: In What Context Did Trichromatic Color Vision Evolve In Primmentioning

confidence: 99%

The Causes and Consequences of Color Vision

Gerl

Morris

2008

Evo Edu Outreach

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The ability to see colors is not universal in the animal kingdom. Those animals that can detect differences in the wavelengths of the electromagnetic spectrum glean valuable sensory information about their environment. They use color vision to forage, avoid predators, and find highquality mates. In the past, the colors that humans could see clouded scientists' study of animals' color perception. Leaving that bias behind has led to new insights about how and why the color vision of animals evolved. This paper provides a brief introduction to color vision, the genetics of color vision in humans, what colors other animals see, and how scientists study color vision. We examine the consequences of having color vision, including speciation, loss of olfactory capabilities, and sexual selection.

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Evolution and selection of trichromatic vision in primates

Cited by 280 publications

References 65 publications

Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates

Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates

The evolution of pheromonal communication

The Causes and Consequences of Color Vision

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