MBE Advance Access published online on October 27, 2009
Molecular Biology and Evolution, doi:10.1093/molbev/msp262
Research Article |
An explicit signature of balancing selection for color vision variation in New World monkeys
* Department of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa 277-8562, Japan
Department of Anthropology, University of Calgary, Calgary AB T2N 1N4, Canada
Psychology Department, University of Chester, Chester CH1 4BJ, United Kingdom
Research Centre in Evolutionary Anthropology and Palaeoecology, School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool L3 3AF, United Kingdom
|| Department of Evolutionary Studies and Biosystems, The Graduate University for Advanced Studies (SOKENDAI), Hayama 240-0193, Japan
Corresponding author: Dr. Shoji Kawamura, Department of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Seimeitou 502, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8562, Japan, Tel: +81-4-7136-5422, Fax: +81-4-7136-3692, E-mail: Kawamura{at}k.u-tokyo.ac.jp
Received for publication July 25, 2009. Revision received September 30, 2009. Revision received October 22, 2009. Revision received October 23, 2009. Accepted for publication October 24, 2009.
Color vision is an important characteristic of primates and, intriguingly, Neotropical monkeys are highly polymorphic for this trait. Recent field studies have challenged the conventional view that trichromatic color vision is more adaptive than dichromatic color vision. No study has investigated the pattern of genetic variation in the long to middle-wavelength sensitive (L-M or red-green) opsin gene as compared to that of other genomic regions (neutral references) in wild populations of New World monkeys to look for the signature of natural selection. Here we report such a study conducted on spider monkeys and capuchin monkeys inhabiting Santa Rosa National Park, Costa Rica. The nucleotide sequence of the L-M opsin gene was more polymorphic than the sequences of the neutral references, although the opsin gene sequences were not more divergent between the two species than were the sequences of the neutral references. In a coalescence simulation that took into account the observed nucleotide diversity of the neutral references, the Tajima's D value of the L-M opsin gene deviated significantly in a positive direction from the expected range. These results are the first to statistically demonstrate balancing selection acting on the polymorphic L-M opsin gene of New World monkeys. Taking the results of behavioral and genetic studies together, the balancing selection we detected may indicate that coexistence of different color vision types in the same population, also characteristic of humans, is adaptive.
Key Words: opsin • color vision polymorphism • balancing selection • New World monkeys • Ateles geoffroyi • Cebus capucinus
1 Present address: Division of Sensory and Cognitive Information, National Institute for Physiological Science, Okazaki 444-8585, Japan