The Heterozygote Superiority Hypothesis for Polymorphic Color Vision Is Not Supported by Long-Term Fitness Data from Wild Neotropical Monkeys

Abstract

The leading explanatory model for the widespread occurrence of color vision polymorphism in Neotropical primates is the heterozygote superiority hypothesis, which postulates that trichromatic individuals have a fitness advantage over other phenotypes because red-green chromatic discrimination is useful for foraging, social signaling, or predator detection. Alternative explanatory models predict that dichromatic and trichromatic phenotypes are each suited to distinct tasks. To conclusively evaluate these models, one must determine whether proposed visual advantages translate into differential fitness of trichromatic and dichromatic individuals. We tested whether color vision phenotype is a significant predictor of female fitness in a population of wild capuchins, using long-term (26 years) survival and fertility data. We found no advantage to trichromats over dichromats for three fitness measures (fertility rates, offspring survival and maternal survival). This finding suggests that a selective mechanism other than heterozygote advantage is operating to maintain the color vision polymorphism. We propose that attention be directed to field testing the alternative mechanisms of balancing selection proposed to explain opsin polymorphism: niche-divergence, frequency-dependence and mutual benefit of association. This is the first in-depth, long-term study examining the effects of color vision variation on survival and reproductive success in a naturally-occurring population of primates.