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

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

  • Linda M. Fedigan, 
  • Amanda D. Melin, 
  • John F. Addicott, 
  • Shoji Kawamura
PLOS
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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.

Introduction

The allelic trichromacy of longtomiddle wave sensitive LM 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. Since its discovery approximately 30 years ago, this color vision polymorphism has intrigued evolutionary biologists and led to extensive debate about its utility in social signaling and finding foods, and about the nature of natural selection behind it e.g., [3][5]. Most Neotropical primates possess variable color vision resulting from the polymorphic sexlinked LM opsin gene and a monomorphic autosomal shortwave sensitive S opsin recently reviewed by Jacobs [6]. Females heterozygous for the LM opsin are capable of trichromatic vision, whereas the remaining homozygous females and all males are dichromatic, a condition known in humans as redgreen color blindness [7].

A large and growing body of research has documented 1 that conemediated color vision phenotype can be predicted in a straightforward manner from the opsin genotype, and 2 that there are clear behavioral correlates of variable color vision e.g., [8][11]. Yet the evolutionary mechanism maintaining color vision polymorphism remains unknown. In the case of the LM polymorphism, we can rule out drift or random effects with a fair amount of certainty as Hiwatashi etal. [2] documented convincing support for balancing selection on the gene in question. Several hypotheses, drawn from the wider range of evolutionary mechanisms under which genetic polymorphisms are maintained via natural selection [12], have been specifically proposed to explain the maintenance of opsin polymorphisms in primates [3], [4], [13], [14].

The most widely accredited explanatory model, the heterozygote superiority overdominance hypothesis, makes the assertion that individuals with trichromatic vision females heterozygous for the LM opsin have a fitness advantage relative to homozygous genotypes, since redgreen chromatic discrimination is useful in foraging for reddish, conspicuous fruits [15][18] or young leaves [19] for sociosexual signaling via pelage color [20] or patterns of blood flow [21] or for detecting items of importance in the environment, including sympatric primate species and predators such as tropical felids [22], [23,] Figure 1. Indeed, we have shown that trichromatic females in a population of wild whitefaced capuchins Cebus capucinus are more accurate in selecting ripe, reddish fruits than are males or dichromatic females [24]. However, that improved accuracy did not translate to a net increase in feeding rate, perhaps because dichromats used behavioral compensation, had improved color perception in certain light environments or increased their reliance on other sensory modalities, such as olfaction [25][27]. Similar results for a sympatric population of polymorphic spider monkeys, documenting no difference in fruit feeding rates between dichromatic and trichromatic monkeys, are reported by Hiramatsu etal. [25], [26], and by Vogel etal. [28] in their study of a neighboring population of whitefaced capuchins.

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Figure 1. How female capuchins see the world.

Color vision phenotype affects perception of relevant objects in the natural environment, including sympatric primates top row, Ateles geoffroyi, photo credit F. Campos, ripe dietary fruits middle row, Ficus ovalis, photo credit A. Melin and predators bottom row, Puma concolor, photo credit N. Parr. Renditions of dichromatic vision left column of images were generated via a computer program customized to simulate primate color vision [55] and were based on the most common dichromatic capuchin phenotype LM allele with peak sensitivity of 561nm.

http://dx.doi.org/10.1371/journal.pone.0084872.g001

The other explanatory models niche divergence, negative frequencydependent selection, and mutual benefit of association share overlapping predictions contingent on dichromatic and trichromatic phenotypes each being suited to distinctive tasks [3], [5]. For example, dichromats are reported to excel at breaking camouflage caused by variegated backgrounds [29], [30], which assists them in detecting cryptic predators and prey. Additionally, studies of New World monkeys have shown that dichromatic females and males are more efficient than are trichromats at detecting and capturing camouflaged objects e.g., insects especially under low ambient light conditions [31][34]. Divergent abilities due to vision phenotype could therefore allow individuals to specialize on different foods and decrease intragroup feeding competition. Monkeys with rare phenotypes might be especially favored if they experience the least competition for their preferred food type. As social organisms, dichromatic monkeys may also benefit from coresiding with trichromats who lead the group to conspicuously colored fruit trees [18] or who first spot yellowish felids [23]. In turn, trichromats may benefit from capturing camouflaged insects flushed by dichromatic group members [35], or by hearing their alarm calls given to cryptic predatory snakes.

As noted by Cropp etal. [36], it is premature to choose among these adaptationist explanations without studies that examine fitness variability among individuals of different phenotypes. Similarly, Surridge etal. [4] have argued that researchers need to conduct studies to determine whether the proposed visual advantages experienced by trichromats or dichromats actually translate into increased survival and reproductive success. The goal of our paper is to provide such a comparative report on fitness in the trichromatic and dichromatic females of a wild population of Costa Rican whitefaced capuchins. We have previously documented a triallelic LM opsin gene polymorphism in this population, individual members of which exhibit one of three dichromatic phenotypes that are traditionally named after the peak spectral sensitivity of their LM photopigments Red 561nm, Yellow 543nm or Green 532nm, or one of three trichromatic phenotypes GreenRed, GreenYellow, RedYellow [2], [37]. We predict that if the LM polymorphism is maintained via heterozygote superiority, then trichromatic females should have better survival or greater reproductive success than do dichromatic females. Alternatively, if overdominance is not operating and the polymorphism is maintained by an alternate mechanism, then we predict that trichromatic and dichromatic females will have similar overall fitness.

Research on differential reproductive success in wild primates has examined many possible predictors and come to often contradictory results as to the effects of dominance rank, maternal age, infant sex, resource availability and group size on variable fitness of individuals, see review by Pusey [38]. Although age and dominance rank of the mother are often good predictors of reproductive success across many primate species, this is not true in all primate populations and our previous analyses have shown that both maternal age and rank fail to predict female reproductive success in our study animals [39], perhaps because of the confounding effects of frequent aggressive invasions of groups and associated infanticide by immigrating capuchin males [40], [41]. However, the production and survival rates of a female capuchins infants are well predicted by the number of matrilineal kin and by the adult male female ratio in her group higher ratio of resident adult males predicts greater female reproductive success, as well as by the availability of resources and whether or not her previous infant survived past one year of age [42].

In the present study, we build on previous work examining differential reproductive success in primates by testing whether color vision phenotype is a significant predictor of female fitness in wild whitefaced capuchin monkeys. We also build on previous tests of the overdominance hypothesis that found no trichromat advantages in fruit feeding rates [2426], by here providing a conclusive test of whether proposed trichromatic visual advantages translate to enhanced fitness in our study animals.

Methods

Ethics Statement

The research reported in this study adhered to protocols approved by the Canada Council for Animal Care through the University of Calgarys Life and Environmental Animal Care Committee LESACC, protocol numbers AC110082, BIO8203, BI 200803, BI 200507, BI 200208, and the University of Albertas Biosciences Animal Care Committee protocol numbers 610151, 151804, 319104. Our research also adhered to the laws of Costa Rica and was conducted with permission from the administrators of the rea de Conservacin Guanacaste and the National Park Service of Costa Rica ACGPI0262013.

We have submitted research protocols on annual applications to the University of Calgarys and the University of Albertas Animal Care Committees and they have approved all the protocols that we used to collect the data analyzed in this study i.e., observational data collection on behavior, births, naturallyoccurring mortality and collection of fecal samples. The analyses in this paper are based on 26 years of life history data births and naturallyoccurring deaths as well as color vision genetics data extracted from fecal samples. Fecal samples are collected noninvasively from the ground below the trees or lowlying vegetation following the defecation of an individual monkey. The monkeys of Santa Rosa are a naturallyoccurring population, freeliving in a national park and no monkeys were handled or interacted with during this study.

Study Species and Site

Whitefaced capuchins Cebus capucinus occur in Central and South America from Honduras at the northern edge of their range down to the northwestern corners of Ecuador and Colombia in the south. They are arboreal omnivores that can survive in a variety of habitats and consume an eclectic diet of fruit, flowers, pith, invertebrates and small vertebrates. They live in multimale, multifemale groups made up of natal females, immigrant males and their offspring. Parkwide censuses of all the capuchin groups in Santa Rosa indicate an average group size of 17 and an overall adult sex ratio approaching 11 [43]. Males disperse from their natal group around the age of 4.5 and continue to move between groups approximately every four years, sometimes alone and sometimes in parallel with their male kin e.g., siblings, cousins [44], [45]. Males sometimes immigrate into groups peacefully when they are not fully grown or when the group has been vacated by the resident males, but most adult and subadult males enter groups by force in coalitions that challenge and drive the prior resident males from the group [41]. During and soon after these aggressive takeovers, many group members are injured and infants often die. Infanticide is the major source of mortality in the first year of life [40].

Females on the other hand, remain in their natal groups, except for a few individuals 12 who occasionally leave with the former resident alpha male when he departs the group, and together they join a neighboring group [46]. Females first give birth at the mean age of 6.5 years and there is little variation around age at first birth 5.9 to 7.3 years 68 of females first give birth in their sixth year of life. Subsequent to first parturition, females typically give birth every two years thereafter unless the first infant dies, in which case the interbirth interval averages 1 year. Female rank does not affect interbirth interval length and dominance rank is not a lifelong characteristic of individual monkeys [39].

The site of our study, Santa Rosa National Park in Costa Rica, was established in 1971 and encompassed 108 km2 of tropical dry forest before it was amalgamated in the late 1980s with small neighboring parks and ranchlands into the megapark, rea de Conservacin Guanacaste ACG. The core of ACG remains as Sector Santa Rosa, which is the location of the capuchin groups that we have studied since 1983. Detailed description of this site and species as well as life history and census data on the Santa Rosa capuchins can be found in Fedigan and Jack [43].

Study Sample and Determination of Color Vision Phenotype

The data analyzed herein come from four closelystudied and contiguous social groups of Santa Rosa capuchins CP, LV, EX and GN on which we have up to 26 years of life history data. These groups have been continuously monitored since their startofstudy dates CP 19832012 LV 19902012 GN EX 20072012 with the exception of seven gaps in CP and LV data collection lasting 26 months each most gaps were two months in length. Birth dates of 15 infants born during these gaps were estimated based on their morphology when we first encountered them and our extensive experience with approximately 140 infants that we have observed closely since the exact day or week of their birth. Death dates of monkeys that disappeared during the gaps were assigned as the midpoint of the period. It is possible that we missed some infants that were born and died during these short periods when groups were not monitored. When new researchers joined our team, they were trained in the field until they could reliably recognize all individuals, ensuring continuity and accuracy of identity and age assignments. Following this method, we have collected data on wellknown monkeys over their complete lifetimes and up to five generations of females have been observed in CP group.

Thus far, we have tracked the survival and reproductive lives of 101 females living in these four adjacent groups. Of these, we determined the color vision phenotype for 49 females 21 dichromats, 28 trichromats. Fortyeight of these 49 colortyped individuals lived beyond two years of age and were included in the longevity postweaning survival analysis. Thirtyseven females produced infants 17 dichromatic and 20 trichromatic mothers and were included in the reproductive analyses Table 1. Among the trichromatic mothers, the GreenRed phenotype was most common and among the dichromatic mothers, the Red phenotype was most common Table 1.

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Table 1. Female Capuchin Color Vision Phenotypes, Survivorship, and Production of Infants. ML pigment sensitivity describes the peak spectral sensitivity max of the constituent middletolong wavelength sensitive photopigments red561nm, yellow543nm, green532nm.

We performed color vision genotyping from fecal DNA collected noninvasively. Multiple 25 fecal samples were collected from all individuals in each social group. Approximately 1gm of feces was stored at ambient temperature in 5ml of ASL buffer QIAamp DNA Stool Mini Kit Qiagen, predispensed into sterile 15ml plastic vials. Fecal DNA was isolated using the QIAamp DNA stool mini kit Qiagen Inc. in a biological safety cabinet. We sequenced the LM opsin genes of each individual from a minimum of two different fecal samples, requiring two identical results to assign a color vision genotype. Entire gene sequences of the three alleles of Cebus capucinus were registered in GenBank in 2005 under accession numbers AB193773 P561 allele, AB193778 P543 allele and AB193784 P532 allele. Amino acid residues at the three critical tuning sites exon 3, site 180 exon 5 sites 277 and 285 were determined to assign the color vision genotype [26]. We minimized the chances of allelic dropout by requiring that at least one fecal sample from each female contained no less than 200pg of genomic DNA. Further details, including our PCR and sequencing protocols, are described in previous publications [24], [26].

Measures of Fitness and Reproductive Success

The rate of infant production fertility and survival of those infants, and longevity of the mother herself, are three important components of female fitness [38], [47], [48]. We address these three variables in turn.

In iteroparous organisms that habitually give birth to one infant at a time most primates, fertility rates depend on the length of time between parturition events, i.e., the interbirth interval, or IBI [49]. We calculated the intervals between live births as our measure of fertility rate. IBIs are commonly used in primatology as a proxy for the number of infants born per female in a given time interval [38], [50], and since our data on births were unavoidably constrained by the arbitrary start and stop dates of our study, it was more appropriate to use IBIs rather than number of infants born as our measure of female fertility. We included in our analyses intervals that were right censored by the stop date of our study or deathdeparture of the mother, since their exclusion may result in systematic bias toward shorter intervals [51]. Furthermore, our previous finding that death of an infant prior to 1year of age shortens the length of the interbirth interval [39] led us to distinguish between intervals in which the first infant died prior to the age of 1year and those in which the first infant survived. By separating out IBIs in which the first infant died prematurely, we were also able to remove any effects of early infant deathinfanticide on IBI length.

To be reproductively successful, a female primate needs not only to produce infants but also to experience high rates of survival in her offspring and to live a comparatively long life herself. We examined the survival of a females infants from their births to two years of age. We used age two as the cutoff point for calculating offspring survival on the assumption that prior to this age, an immature monkeys survival would be primarily a function of their mothers rather than their own color vision phenotype. This is because in the first year or two of life, prior to weaning, a young capuchin depends on its mother for milk and because the mothers ecological fitness and health determine the availability of her milk and the amount of care e.g., transportation and protection she can provide to the infant.

Our second measure of survival was that of the mother herself longevity which we calculated from two years of age i.e. postweaning until her death or the end of our study. Sometimes we find the cadaver of a deceased study animal on the forest floor, or we observe them to be wounded or ill before they disappear, in which case we record them as dead. Females seldom disperse 12 of females have emigrated out of, or immigrated into our study groups and in the few cases where females have dispersed from our study groups, we have tracked them to a neighboring group. Therefore, we assume that any cases of postweaning female disappearances are deaths.

For both IBIs and the survival of infants, we accounted for potential autocorrelations in the fitness events experienced by each particular mother by introducing a random effect of the identity of the mother in the analyses. As noted by Jones etal. [49], introducing the random effect of the mothers identity also provides an indirect measure of phenotypic quality or frailty.

Statistical Analyses

To assess the pace of infant production, we used mixed effects Cox regressions coxme and coxph procedures [52] in R [53] and analyzed the length of 139 interbirth intervals IBIs, Table 1. There were a total of 101 completeuncensored and 38 censored intervals for 37 mothers of known visual phenotypes. The model included IBI as the dependent variable, a fixed effect of the mothers color vision phenotype dichromatic or trichromatic, a fixed effect of whether the first infant in the interval died prior to age 1, and a random effect of the identity of the adult female. Censored values included cases where the female was still alive at the end of the study but had not yet given birth to another infant and cases where a female had died. Thus, if a female had N births, there were N values for IBI, the first being the interval between births 1 and 2, and the last being the censored interval between last birth and deathend of study.

To determine the effect of the mothers color vision type and of the mothers identity on the survival of her infants, we used mixed effects Cox regressions combining coxme and coxph procedures in R to analyze the survival of infants from birth to age 2. We included all 139 infants born to 37 females with known color vision phenotypes Table 1. The model included age of the infant at death or at the end of the study if the infant was still alive but less than 2 years of age, as well as a fixed effect of the mothers color vision type and a random effect for the identity of the adult female.

To examine the longevity of trichromatic versus dichromatic females, we used a Cox proportional hazard regression the coxph procedure in R to analyze the survival of individual females from the age of two years on. There were a total of 48 females included in this analysis for which we know their color vision phenotype and that they survived beyond two years of age Table 1. The model included a survival function for the females as a function of being trichromatic or dichromatic. The age at death was rightcensored for those individuals still alive at the end of the study. The age of entry into the study was left censored if the individual did not enter the study at birth in which case we estimated her age, based on agerelated morphological features such as brow and nipple length, and based on 26 years of observing the aging process in females of known age.

Because the advantage proposed to exist for trichromats is hypothesized to be particularly strong for those that have maximum sensitivity near the green or red end of the spectrum, we repeated all three analyses IBI, offspring survival, maternal survival, using only reproductive data from GreenRed trichromats and comparing them to dichromats.

Results

Interbirth Interval Duration in Trichromatic versus Dichromatic Females

We examined the length of interbirth intervals IBIs N139 as a function of the effect of 1 the mothers color vision phenotype 2 the death of the first infant in the interval at 1year of age and 3 the random effect of the mothers identity. The interbirth intervals of trichromatic versus dichromatic females did not differ significantly 20.445, df1, p0.504, Figure 2. For IBIs where the first infant in the interval lived at least one year, the fitted median IBI was 2.05 years N56 for trichromatic females and 2.19 years N45 for dichromatic females.

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Figure 2. Cumulative Hazard functions for interbirth intervals IBI as a function of time in years for females with dichromat color vision dashed lines and trichromat color vision solid lines and for IBIs in which the first infant in the interval did left lines or did not right lines die at 1year.

Cumulative hazard represents the probability that an interbirth interval ends on or before a particular age. Dots represent censored IBIs i.e., those IBIs where the female died prior to the next birth or where at the end of the study period the female had not yet given birth again.

http://dx.doi.org/10.1371/journal.pone.0084872.g002

In accordance with a previous study [39], we found that interbirth intervals in which the first infant died before age 1 were significantly shorter than intervals in which the first infant survived 259.5, df1, P0.001 and this was true for both trichromats and dichromats Figure 2. For IBIs where the first infant in the interval died before age 1, the fitted median IBI was 1.01 years N28 for trichromatic females and 1.13 years N10 for dichromatic females.

Finally, we found that the individual identity of the mother i.e., the random effect of the mother independent of her vision phenotype contributed significantly to the explanatory power of the model 24.460, df1, p0.035.

Survival of Infants Born to Trichromatic versus Dichromatic Mothers

We assessed the survival of infants N139 from birth to the age of two years, the typical timing of weaning, as a fixed effect of the mothers color vision phenotype and the random effect of the mothers identity. Infants of trichromatic mothers did not live longer up to two years than those born to dichromatic mothers 21.49, df1, p0.221, nor did the identity of the mother contribute to explaining variation in the probability of the offspring surviving to the age of two 20.005, df1, p0.940, Figure 3. For trichromatic females, 61.9 of their offspring survived to age 2, whereas for dichromatic females, 79.6 of their offspring survived to age 2.

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Figure 3. Survival of dependent offspring between birth and age two in years as a function of mothers color vision type dichromat dashed line or trichromat solid line.

Dots represent censored observations i.e., those individuals that were still alive and less than 2 years of age at the end of the study.

http://dx.doi.org/10.1371/journal.pone.0084872.g003

Survival of Trichromatic versus Dichromatic Females Post Weaning

When we examined the survival of females past the age of 2 years as a function of their color vision phenotype we found that survival did not differ between trichromats and dichromats 20.91, df1, p0.339, Figure 4. The median predicted survival time for dichromatic females was 22.1 years N20 and 19.8 years for trichromats N28. Additionally, if we consider only those females who actually died before the end of our study, we can see from Table 1 that they lived between 1.21 and 26.75 years. The mean age of survival for the trichromatic females who died before the end of the study n11 was 11.99 years and the mean age of survival for dichromatic females who died N5 was 11.46 years.

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Figure 4. Survival of females from 2 years of age as a function of their color vision type dichromats dashed line trichromats solid line.

Dots represent censored observations i.e., those individuals that were alive and older than 2 years of age at the end of the study.

http://dx.doi.org/10.1371/journal.pone.0084872.g004

Comparison of GreenRed Trichromats to Dichromats for Interbirth Intervals, Offspring Survival and Maternal Survival

Because the LM photopigments of GreenYellow and RedYellow trichromats are less spectrallyseparated equivalent to anomalous trichromacies in humans than the photopigments of GreenRed trichromats, it is possible that the former phenotypes might experience lower fitness and bring down the trichromatic group mean. To test for this, we performed the same analyses as those presented above, but this time we limited the sample of trichromats to the GreenRed phenotype.

We found that the results for all of these analyses were qualitatively identical to those presented above for the trichromatdichromat comparison. There were no significant differences between GreenRed trichromats and dichromats on any of our three measures of female fitness. Specifically, the phenotype of the mother GreenRed trichromat versus dichromat has no discernible effect on the length of her IBI 21.41, df1, p0.234, and the early death of the first offspring in an IBI leads to a shorter IBI for both GreenRed trichromats and dichromatic mothers 234.0, df1, p0.001. Second, the mothers vision phenotype does not affect the offsprings survival up to 2 years 22.54, df1, p0.109. Third, the survival of females after the age of 2 is not significantly affected by their vision phenotype 23.66, df1, p0.055 and the trend is in the direction of dichromats surviving better than the GreenRed trichromats.

Discussion

Although 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. Not only did the differences fail to reach significance, the trends for infant and maternal survival were in the opposite direction than predicted by the heterozygote superiority hypothesis Figures 3 4. The one clear and consistent prediction from the literature is that GreenRed trichromats should experience visual advantages and therefore fitness advantages in comparison to the five other phenotypes found in capuchins, and in particular GreenReds should do better than the dichromats [54][60]. However, even when we limited our analyses to the GreenRed trichromat females, there was no indication whatsoever that greenred trichromatic females do better than dichromats on any measure of fitness fertility rates, offspring survival, maternal survival. We suggest therefore that an alternate selective mechanism is operating to maintain color vision polymorphism in our study animals.

Despite the lack of fitness differences due to color vision phenotype, we did find significant variation in IBIs attributable to the mothers identity, indicating that some aspect of phenotypic quality, other than color vision, is influential in the pace of infant production in our capuchins. These results are in accordance with other recent studies on female primates e.g., 49 in which the effect of the mothers identity was investigated. Dominance rank and age are unlikely to explain these characteristic IBI lengths that are consistent over a females lifetime, in particular because rank and age change over the course of a female capuchins life and because our previous studies of the effects of dominance and age failed to demonstrate that these variables are significant predictors of IBI length in our study animals [39]. However, other aspects of a females behavior may affect her lifelong fertility pattern, in that some females may consistently behave in ways to enhance their probability and frequency of producing offspring. For example, they may act strategically to achieve more conceptive matings or to acquire higherquality resources that enhance fertility.

Thus, this study has demonstrated that there is individual heterogeneity in at least one component of fitness in female capuchins length of the interbirth interval but that variability appears not to be driven by a superiority of the trichromatic phenotype, even when we factor out the effects of early infant deaths. Hiwatashi etal. [2] report a clear indication that balancing selection is maintaining color vision polymorphism in these same study animals yet our analyses show that this polymorphism does not result in differential fitness of trichromats over dichromats, which suggests that evolutionary ecologists should turn their attention to deriving testable predictions from the alternate hypotheses for mechanisms of balancing selection, all of which postulate that multiple color vision phenotypes each have their own advantages under distinct ecological or social conditions.

A surprising dearth of attention has been directed towards evaluating the three alternate mechanisms that have been proposed to explain intraspecific opsin polymorphism nichedivergence, frequencydependence, and mutual benefit of association. In part, this may be due to the difficulty of teasing apart these hypotheses due to their largely overlapping predictions. To our knowledge, only one field study has directly addressed an alternate hypothesis. Melin etal. [13] concluded that nichedivergence in diet is unlikely to be operating on polymorphic color vision in Santa Rosa capuchins due to the similarity of diet composition across group members that is driven by cohesive group behaviors. However, the scope of this study was restricted to broad categorizations of food types. A more detailed and nuanced examination of niche differentiation by dichromats and trichromats, including canopy use e.g., [17], [61] and finer dietary categorization, may reveal important differences. Furthermore, future work should investigate the extent of communal resource discovery and use, versus individual detection and monopolization of foods. Finally, it will be prudent moving forward to assess the importance of visual tasks unrelated to foraging, such as predator detection, which may be an important factor under a mutualbenefit of association scenario.

In their review article on linking genotypes, phenotypes and fitness, Bradley and Lawler [11] note that it is an open question as to how shortterm differences in foraging skills of dichromatic versus trichromatic primates translate to differences in ultimate fitness. Our study suggests that the distinctive foraging skills of dichromatic and trichromatic whitefaced capuchins each confer their own advantages such that neither phenotype has an overarching fitness benefit.

Acknowledgments

We thank the Costa Rican National Park Service and administrators of the rea de Conservacin Guanacaste especially Roger Blanco Segura for permission to conduct research in the park since 1983. Many students, colleagues and field assistants have contributed to the longterm life history database we maintain on the Santa Rosa capuchins and we thank them all. Greg Bridgett and Neil Griffin assisted in preparation of the manuscript. We also thank the editor, Dr. Elsa Addessi, as well as Dr. Daniel Pessoa and one anonymous reviewer, for their comments on previous versions of this paper.

Author Contributions

Conceived and designed the experiments LMF ADM JFA SK. Performed the experiments LMF ADM. Analyzed the data JFA. Wrote the paper LMF ADM JFA SK.

References

  1. 1. Surridge AK, Mundy NI (2002) Transspecific evolution of opsin alleles and the maintenance of trichromatic color vision in Callitrichine primates. Mol Evol 11: 2157–2169. doi: 10.1046/j.1365-294x.2002.01597.x
  2. 2. Hiwatashi T, Okabe Y, Tsutsui T, Hiramatsu C, Melin AD, et al. (2010) An explicit signature of balancing selection for colorvision variation in new world monkeys. Mol Biol Evol 27: 453–464. doi: 10.1093/molbev/msp262
  3. 3. Mollon JD, Bowmaker JK, Jacobs GH (1984) Variations of color vision in a New World primate can be explained by polymorphism of retinal photopigments. Proc R Soc Lond B Biol Sci 222: 373–399. doi: 10.1098/rspb.1984.0071
  4. 4. Surridge AK, Osorio D, Mundy NI (2003) Evolution and selection of trichromatic vision in primates. Trends Ecol Evol 51: 198–205. doi: 10.1016/s0169-5347(03)00012-0
  5. 5. Melin AD, Hiramatsu C, Fedigan LM, Schaffner CM, Aureli F, Kawamura S 2012 Polymorphism and adaptation of primate color vision. In Pontarotti P, ed. Evolutionary Biology Mechanisms and Trends. Heidelberg SpringerVerlag. 225241.
  6. 6. Jacobs GH (2009) Evolution of colour vision in mammals. Philos Trans R Soc Lond B. 364: 2957–2967. doi: 10.1098/rstb.2009.0039
  7. 7. Sharp LT, Stockman A, Jagle H, Nathans J 1999 Opsin genes, cone photopigments, color vision and color blindness. In Gegenfurtner KR, Sharpe LT, eds. Color vision from genes to perception. New York Cambridge Univ. Press. 351.
  8. 8. Deeb S, Lindsey D, Hibiya Y, Sanocki E, Winderickx J, et al. (1992) Genotypephenotype relationships in human redgreen colorvision defects molecular and psychophysical studies. Am J Hum Genet 51: 687–700.
  9. 9. Caine NG, Mundy NI (2000) Demonstration of a foraging advantage for trichromatic marmosets Callithrix geoffroyi dependant on food colour. Proc R Soc Lond B Biol Sci 267: 439–444. doi: 10.1098/rspb.2000.1019
  10. 10. Saito A, Kawamura S, Mikami A, Ueno Y, Hiramatsu C, et al. (2005a) Demonstration of a genotypephenotype correlation in the polymorphic color vision of a noncallitrichine New World monkey, capuchin Cebus apella.. Am J Primatol 67: 471–485. doi: 10.1002/ajp.20201
  11. 11. Bradley BJ, Lawler RR (2011) Linking genotypes, phenotypes, and fitness in wild primate populations. Evol Anthropol 20: 104–119. doi: 10.1002/evan.20306
  12. 12. Hartl DL, Clark AG 2007 Principles of Population Genetics, 4th Edition. Sunderland, Sinauer.
  13. 13. Melin AD, Fedigan LM, Hiramatsu C, Kawamura S (2008) Polymorphic color vision in whitefaced capuchins Cebus capucinus Is there foraging niche divergence among phenotypes. Behav Ecol Sociobiol 62: 659–670. doi: 10.1007/s00265-007-0490-3
  14. 14. Kawamura S, Hiramatsu C, Melin AD, Aureli F, Fedigan LM, et al.. 2012 Polymorphic color vision in primates evolutionary considerations. In Hirai H, Imai H, Go Y, eds. Post Genome Biology of Primates. Tokyo Springer Press. pp. 93120.
  15. 15. Mollon JD (1989) Tho she kneeld in that place where they grew The uses and origins of primate color vision. J Exp Biol 146: 21–38.
  16. 16. Sumner P, Mollon JD (2000) Chromacy as a signal of ripeness in fruits taken by primates. J Exp Biol 203: 1987–2000.
  17. 17. Regan BC, Julliot C, Simmen B, Vienot F, CharlesDominique P, et al. (2001) Fruits, foliage and the evolution of primate colour vision. Philos Trans R So. Lond B 356: 229–283. doi: 10.1098/rstb.2000.0773
  18. 18. Smith AC, BuchananSmith HM, Surridge AK, Mundy NI (2003) Leaders of progressions in wild mixedspecies troops of saddleback Saguinus fuscicollis and mustached tamarins S. mytax with emphasis on color vision and sex. Am J Primatol 61: 145–157. doi: 10.1002/ajp.10117
  19. 19. Dominy NJ, Lucas PW (2001) Ecological importance of trichromatic vision to primates. Nature 4106826: 363–366.
  20. 20. Kamilar JM, Heesy CP, Bradley BJ (2013) Did trichromatic color vision and red hair coevolve in primates. Am J Primatol 75: 740–751. doi: 10.1002/ajp.22099
  21. 21. Changizi MA, Zhang Q, Shimojo S (2006) Bare skin, blood and the evolution of primate color vision. Biol Lett 2: 217–221. doi: 10.1098/rsbl.2006.0440
  22. 22. Caine NG 2002 Seeing red consequences of indvidual differences in color vision in callitrichid primates. In Miller LE, ed. Eat or Be Eaten. Cambridge Cambridge Univ. Press. 5873.
  23. 23. Sumner P, Mollon JD (2003) Colors of primate pelage and skin objective assessment of conspicuousness. Am J Primatol 59: 67–91. doi: 10.1002/ajp.10066
  24. 24. Melin AD, Fedigan LM, Hiramatsu C, Hiwatashi T, Parr N, et al. (2009) Fig foraging by dichromatic and trichromatic Cebus capucinus in a tropical dry forest. Int J Primatol 30: 753–775. doi: 10.1007/s10764-009-9383-9
  25. 25. Hiramatsu C, Melin AD, Aureli F, Schaffner CM, Vorobyev M, et al. (2009) Interplay of olfaction and vision in fruit foraging of spider monkeys. Anim Behav 77: 1421–1426. doi: 10.1016/j.anbehav.2009.02.012
  26. 26. Hiramatsu C, Melin AD, Aureli F, Schaffner CM, Vorobyev M, et al. (2008) Importance of achromatic contrast in shortrange fruit foraging of primates. PLoS One 3: 1–12. doi: 10.1371/journal.pone.0003356
  27. 27. Freitag FB, Pessoa DMA (2012) Effect of luminosity on color discrimination of dichromatic marmosets Callithrix jacchus. J Optical Soc Amer AOptics Image Sci and Vision 29: A216–A222. doi: 10.1364/josaa.29.00a216
  28. 28. Vogel E, Neitz M, Dominy N (2007) Effect of color vision phenotype in the foraging of whitefaced capuchins, Cebus capucinus. Behav Ecol 18: 292–297. doi: 10.1093/beheco/arl082
  29. 29. Morgan MJ, Adam A, Mollon JD (1992) Dichromats detect colourcamouflaged objects that are not detected by trichromats. Proc Royal Soc Lond B Biol Sci 248: 291–295. doi: 10.1098/rspb.1992.0074
  30. 30. Saito A, Mikami A, Kawamura S, Ueno Y, Hiramatsu C, et al. (2005b) Advantage of dichromats over trichromats in discrimination of colorcamouflaged stimuli in nonhuman primates. Am J Primatol 67: 425–436. doi: 10.1002/ajp.20197
  31. 31. Melin AD, Fedigan LM, Hiramatsu C, Sendall C, Kawamura S (2007) Effects of colour vision phenotype on insect capture by a freeranging population of whitefaced capuchins Cebus capucinus. Anim Behav 73: 205–214. doi: 10.1016/j.anbehav.2006.07.003
  32. 32. Melin AD, Fedigan LM, Young HC, Kawamura S (2010) Can color vision variation explain sex differences in invertebrate foraging by capuchin monkeys. Curr Zool 56: 300–312.
  33. 33. Caine NG, Osorio D, Mundy NI (2010) A foraging advantage for dichromatic marmosets Callithrix geoffroyi at low light intensity. Biol Lett 6: 36–38. doi: 10.1098/rsbl.2009.0591
  34. 34. Smith AC, Surridge AK, Prescott MJ, Osorio D, Mundy NI, et al. (2012) Effect of colour vision status on insect prey capture efficiency of captive and wild tamarins Saguinus spp.. Anim Behav 83: 479–486. doi: 10.1016/j.anbehav.2011.11.023
  35. 35. Montague M, Disotell T, Di Fiore A 2013 Population genetics, dispersal and kinship among wild squirrel monkeys. Preferential association among closelyrelated females and its implications for insect prey capture. Int J Primatol doi 10.1007s1076401397237.
  36. 36. Cropp S, Boinski S, Li WH (2002) Allelic variation in the squirrel monkey xlinked color vision gene biogeographical and behavioral correlates. J Mol Evol 54: 734–745. doi: 10.1007/s00239-001-0073-2
  37. 37. Hiramatsu C, Tsutsui T, Matsumoto Y, Aureli F, Fedigan LM, et al. (2005) Color vision polymorphism in wild capuchins Cebus capucinus and spider monkeys Ateles geoffroyi in Costa Rica. Am J Primatol 67: 447–461. doi: 10.1002/ajp.20199
  38. 38. Pusey A 2012 Magnitude and sources of variation in female reproductive performance. In Mitani JC, Call J, Kappeler PM, Paolombit RA, Silk JB, eds. The Evolution of Primate Societies. Chicago University of Chicago Press. pp. 343366.
  39. 39. Fedigan LM, Carnegie SD, Jack KM (2008) Predictors of reproductive success in female whitefaced capuchins. Am J Phys Anthropol 137: 82–90. doi: 10.1002/ajpa.20848
  40. 40. Fedigan LM (2003) The impact of male takeovers on infant deaths, births and conceptions in Cebus capucinus at Santa Rosa, Costa Rica. Int J Primatol 24: 723–741.
  41. 41. Fedigan LM, Jack KM (2004) The demographic and reproductive contexts of male replacements in Cebus capucinus. Behaviour 141: 755–775. doi: 10.1163/1568539042245178
  42. 42. Fedigan LM, Jack KM (2011) Two girls for every boy the effects of group size and composition on the reproductive success of male and female whitefaced capuchins. Am J Phys Anthropol 144: 317–326. doi: 10.1002/ajpa.21414
  43. 43. Fedigan LM, Jack KM 2012 Tracking monkeys in Santa Rosa lessons from a regenerating tropical dry forest. In Kappeler P, Watts D, eds. Longterm Field Studies of Primates. Heidelberg Spring Verlag. pp. 165184.
  44. 44. Jack KM, Fedigan LM (2004a) Male dispersal patterns in whitefaced capuchins Part 1 patterns and causes of natal dispersal. Anim Behav 67: 761–769. doi: 10.1016/j.anbehav.2003.04.015
  45. 45. Jack KM, Fedigan LM (2004b) Male dispersal patterns in whitefaced capuchins Part 2 patterns and causes of secondary dispersal. Anim Behav 67: 771–782. doi: 10.1016/j.anbehav.2003.06.015
  46. 46. Jack KM, Fedigan LM (2009) Female dispersal in a femalephilopatric species, Cebus capucinus. Behaviour 146: 437–470. doi: 10.1163/156853909x404420
  47. 47. Brown D 1988 Components of lifetime reproductive success. In CluttonBrock TH, ed. Reproductive Success. Chicago University of Chicago Press. 439453.
  48. 48. CluttonBrock TH, Albon SD, Guinness FE 1988 Reproductive success in red deer. In CluttonBrock TH, ed. Reproductive Success. Chicago University of Chicago Press. 325343.
  49. 49. Jones JH, Wilson, Murray C, Pusey A (2010) Phenotypic quality influences fertility in Gombe chimpanzees. J Anim Ecol 79: 1262–1269. doi: 10.1111/j.1365-2656.2010.01687.x
  50. 50. Strier KB (2004) Reproductive strategies of New World primates interbirth intervals and reproductive rates. A Primatol. no Brasil 8: 53–63.
  51. 51. Singer JD, Willett JB 2003 Applied Longitudinal Data Analysis Modeling Change and Event Occurrence. Oxford Oxford University Press.
  52. 52. Therneau T 2012 A Package for Survival Analysis in S. R package version. 2.3614.
  53. 53. R Core Team 2012 R A language and environment for statistical computing. R Foundation for Satistical Computing, Vienna, Austria. ISBN 39000510700, URL http://www.R-project.org.
  54. 54. Melin AD, Young HC, Mosdossy KN, Fedigan LM 2013 The behavioral ecology of color vision considering fruit conspicuity, detection distance and dietary importance. Int J Primatol doi 10.1007s1076401397308.
  55. 55. Melin AD, Kline DW, Hickey C, Fedigan LM (2013) Food search through the eyes of a monkey a functional substitution approach for assessing the ecology of primate color vision. Vision Res 86: 87–96. doi: 10.1016/j.visres.2013.04.013
  56. 56. Osorio D, Smith AC, Vorobyev M, BuchananSmith HM (2004) Detection of fruit and the selection of primate visual pigments for color vision. Am Nat 164: 696–708. doi: 10.1086/425332
  57. 57. RibaHernandez P, Stoner KE, Osorio D (2007) effect of polymorphic color vision for fruit detection in the spider monkey Ateles geoffroyi, andits implications for the maintenance of polymorphic color vision in platyrrhine monkeys. J Exper Biol 207: 2465–2470. doi: 10.1242/jeb.01046
  58. 58. Rowe MP, Jacobs GH (2004) Cone pigment polymorphism in New World monkeys are all pigments created equal. Vis Neurosci 21: 217–222. doi: 10.1017/s0952523804213104
  59. 59. Surridge AK, Suarez SS, BuchananSmith HM, Smith AC, Mundy NI (2005a) Color vision pigment frequencies in wild tamarins Saguinus spp. Am J Primatol 67: 463–470. doi: 10.1002/ajp.20200
  60. 60. Surridge AK, Suarez SS, BuchananSmith HM, Smith AC, Mundy NI (2005b) Nonrandom association of opsin alleles in wild groups of redbellied tamarins Saguinus labiatus and maintenance of the color vision polymorphism. Biol Lett 1: 465–468. doi: 10.1098/rsbl.2005.0367
  61. 61. Yamashita N, Stoner K, RibaHernandez P, Dominy N, Lucas P (2005) Light levels used during feeding by primate species with different color vision types. Behav Ecol Sociobiol 58: 618–629. doi: 10.1007/s00265-005-0936-4