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 redgreen 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 longterm 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 nichedivergence, frequencydependence and mutual benefit of association. This is the first indepth, longterm study examining the effects of color vision variation on survival and reproductive success in a naturallyoccurring population of primates.
Highlights
The allelic trichromacy of long-to-middle wave sensitive (L/M) opsins in New World monkeys is a textbook example of a balanced polymorphism [1,2] and one of the few cases where the fitness consequences of variants living in natural populations are amenable to testing
We examined the length of interbirth intervals (IBIs; N = 139) as a function of the effect of: (1) the mother’s color vision phenotype; (2) the death of the first infant in the interval at,1 year of age; and (3) the random effect of the mother’s identity
Heterozygote superiority appears from the literature to be a widely accepted mechanism explaining primate color vision polymorphism, we found no significant advantage to trichromats over dichromats for the three measures of fitness we examined in female monkeys
Summary
The allelic trichromacy of long-to-middle wave sensitive (L/M) opsins in New World monkeys is a textbook example of a balanced polymorphism [1,2] and one of the few cases where the fitness consequences of variants living in natural populations are amenable to testing. Most Neotropical primates possess variable color vision resulting from the polymorphic sex-linked L/ M opsin gene and a monomorphic autosomal short-wave sensitive (S) opsin (recently reviewed by Jacobs [6]). The evolutionary mechanism maintaining color vision polymorphism remains unknown. In the case of the L/M polymorphism, we can rule out drift or random effects with a fair amount of certainty as Hiwatashi et al [2] documented convincing support for balancing selection on the gene in question. Drawn from the wider range of evolutionary mechanisms under which genetic polymorphisms are maintained via natural selection [12], have been proposed to explain the maintenance of opsin polymorphisms in primates [3,4,13,14]
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