* Department of Ecology and Evolutionary Biology, University of Michigan
Instituto de Neuroetologia and Centro de Investigaciones Tropicales, Universidad Veracruzana, Veracruz, México
Correspondence: E-mail: jianzhi{at}umich.edu.
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Abstract |
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Key Words: TRP2 howler monkey primate pheromone color vision
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Introduction |
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Many genes involved in the VNO pheromone transduction pathway have been identified (Zufall, Kelliher, and Leinders-Zufall 2002; Rodriguez 2003). Among them, the TRP2 gene and pheromone receptor genes appear to be unique to this pathway and thus may be used as genetic markers for studying the evolution of pheromone sensitivity. We chose to study only the TRP2 gene here because pheromone receptor genes form large gene families (Dulac and Axel 1995; Ryba and Tirindelli 1997; Herrada and Dulac 1997; Matsunami and Buck 1997) that are difficult to fully characterize without the availability of a genome sequence. TRP2 is an ion channel of the transient receptor potential family (Liman, Corey, and Dulac 1999). Disruption of the TRP2 gene in mice hampers pheromone perception and causes dramatic changes in sexual and social behaviors (Stowers et al. 2002; Leypold et al. 2002). In all hominoids and OW monkeys surveyed, TRP2 is a pseudogene without an open reading frame (ORF; Zhang and Webb 2003; Liman and Innan 2003). Three of the 13 exons in TRP2 have been sequenced in an individual of Alouatta seniculus, and no ORF-breaking mutations were found (Liman and Innan 2003). But this does not preclude the presence of ORF-breaking mutations in any of the other 10 exons. We here sequenced all 13 exons from three species of howler monkeys. The sequence data, as well as our subsequent evolutionary analysis, suggest that TRP2 is functional in howler monkeys.
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Materials and Methods |
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DNA Sequence Analysis
The complete TRP2 gene sequences of tamarin (Saguinus oedipus), squirrel monkey (Saimiri sciureus), owl monkey (Aotus trivirgatus), saki (Pithecia irrorata), and spider monkey (Ateles geoffroyi) were obtained from Zhang and Webb (2003). The sequences were analyzed based on an established phylogeny of the NW monkeys involved. Ancestral gene sequences at all interior nodes of the tree were inferred by the distance-based Bayesian method (Zhang and Nei 1997). Synonymous and nonsynonymous substitutions were then counted for each tree branch. We also used a likelihood-based method (Yang 1998) to analyze the synonymous and nonsynonymous substitution rates.
Computer Simulation
To examine how long it takes for a nonfunctional TRP2 to lose its ORF, we adopted the computer simulation approach of Zhang and Webb (2003). The speed with which an ORF becomes disrupted depends in large part on the sequence of the ORF, rate of point mutations, and rate of indel (insertion/deletion) mutations. We used a point mutation rate of 2.2 x 10-9 per site per year, as estimated from large genomic data sets of mammals (Kumar and Subramanian 2002). The relative mutational frequencies among the four nucleotides are assumed to be equal, as they have only a negligible effect on the simulation result. We assumed that all indels with sizes that are multiples of three nucleotides (3n indels) do not disrupt an ORF. This simplifies our simulation but does not affect our results, because the majority of indels generated by mutations have small sizes (6 nucleotides; Zhang and Webb 2003). It has been estimated from genomic comparisons between the human and the chimpanzee (Britten 2002) and between human and baboon (Silva and Kondrashov 2002) that the mutation rate of indels is about 1.0 x 10-10 per site per year, of which 17% are 3n indels (Zhang and Webb 2003; Podlaha and Zhang 2003). A simulation was then performed for 20,000 replications with an NW monkey TRP2 coding sequence and the above parameters. Under no functional constraints, the substitution rate is identical to the mutation rate and mutations are assumed to be random. An ORF is interrupted when a non-3n indel or a nonsense point mutation occurs. We thus determined t1/2 of an ORF, or the time required for an intact ORF to be interrupted in half of the simulation replications. The computer program Pseudogene (Zhang and Webb 2003) was used.
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Results |
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Discussion |
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The above conclusion may have two implications: (1) it may indicate that there is no correlation between the presence of trichromacy and lack of pheromone sensitivity, and (2) it may suggest that the phylogenetic concordance of the two traits in non-primate placental mammals, birds, and OW monkeys and hominoids is simply a coincidence. Alternatively, our results may indicate that although trichromacy is related to the loss of pheromone sensitivity, additional factors are also required for the replacement of the pheromone system by color vision. It is worth noting that the origin of trichromacy merely provides a new sensory mechanism, which will have to be coupled with a signaling mechanism to establish a new signaling-sensory channel to replace pheromone communication. In OW monkeys and hominoids, sexual swelling emits the visual signal, and in birds, colorful plumages serve the same function. In NW monkeys, including howlers, no true sexual skins have been found (Dixson 1983). In certain NW monkey species, mild swelling may appear during estrus (Sillen-Tullberg and Moller 1993), but neither the color nor the size of this swelling is comparable to that in OW monkeys and hominoids (Dixson 1983). In open environments, visual signals may be preferred to pheromones because the former can be perceived at a distance whereas the latter requires physical contact. In closed areas such as dense forests, the advantage of visual signals over pheromone signals may diminish, as visual signals are more difficult to transmit. With this difference in mind, it is interesting to note that OW monkeys and hominoids are generally terrestrial and live in more open forests and savannas, while NW monkeys generally live in more dense tropical rainforests and are arboreal (Fleagle 1999). Such ecological differences may have provided a selective advantage for visual signals over pheromone signals in OW but not NW primates, thereby producing the difference in evolutionary force for sexual skin between the two groups of primates.
Taking into account this ecological factor, we propose a revised model of the impact of full trichromacy on the evolution of pheromone sensitivity in primates (fig. 3). According to this model, a critical step, advantage of visual signals over pheromone signals, did not occur in howlers, but occurred in OW monkeys and hominids and led to the difference in pheromone use between the two groups of primates. Further work is required to critically evaluate and possibly test this new model. It is also interesting to note that exaggerated sexual swellings were lost in some OW monkey and hominid species, most of which do not have multi-male social groups (Nunn 1999). Thus, while in our model visual signaling via sexual swelling is prerequisite for the loss of the pheromone sensory system, the visual signal may be subsequently lost in the absence of multi-male mating. It has been suggested that concealed ovulation can be advantageous to females in a single-male mating system, because it will promote paternal care (Sillen-Tullberg and Moller 1993; Nunn 1999).
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Acknowledgements |
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Footnotes |
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Michael Nachman, Associate Editor
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