American Journal of Primatology
RESEARCH ARTICLE The Coevolution of Circumperineal Color and Terrestriality JAMES D. PAMPUSH1* AND JENNIFER D. CRAMER2 1 Department of Anthropology, University of Florida, Gainesville, Florida 2 Department of Sociology, Anthropology, and Women’s Studies, American Military University and American Public University, Charles Town, West Virginia
Old World monkeys (Cercopithecoidea) are unusual among primates for the high percentage of species exhibiting circumperineal coloration, as well as the large percentage of highly terrestrial species. Kingdon [1974,1980] suggested that circumperineal skin coloration is functionally related to terrestriality, but this hypothesis has not been tested. From the literature, we collected data on habitat use (terrestrial/arboreal) and circumperineal coloration (present/absent) for 78 species. Indeed, among the 78 species surveyed here, 75% of them fall into either the category of colored circumperineals with terrestrial lifestyle, or of uncolored circumperineals with arboreal lifestyle (X2(1) ¼ 19.550, P < 0.001). However, conventional statistical procedures assume all taxa are equally related—which is not usually the case in multispecies analyses—leading to higher rates of both type I and II statistical errors. We performed Bayesian trait coevolution analyses that show that models of dependent trait evolution are not signiﬁcantly better than models assuming independent evolution of the two traits (loglikelihood ratio test P ¼ 0.396, Bayes Factor ¼ 1). Bayesian nodal reconstructions of the cercopithecoid phylogeny indicate that relatively few trait transitions are needed to account for the distributions of the two traits. Further, chi-squared distributional tests show that sub-family afﬁliation (i.e., Cercopithecinae, Colobinae) is an accurate predictor of trait status. The discordance of the analyses may represent the results of a few different evolutionary scenarios, but ultimately circumperineal coloration seems weakly linked to terrestrial ecology. Am. J. Primatol. 9999:1–11, 2015. © 2015 Wiley Periodicals, Inc. Key words:
Bayesian analyses; historical contingency; sexual skin; primate predation; pleiotropy
INTRODUCTION Darwin  and other early theorists noted the intriguing and impressive color displays of primates (Fig. 1). Early primate literature was largely descriptive and coloration was typically cataloged as one of many diagnostic features both between and within species [Hill, 1966; Kingdon, 1974; Pocock, 1925; Wickler, 1967]. Field and captive research has expanded our understanding of the role primate color plays in signaling sexual receptivity, social relationships, and rank [see Higham, 2009]. Circumperineal skin color is of particular interest in understanding primate intrasexual competition and intersexual choice. Among primates, colorful skin patches are known to act as signals of competitive ability, quality, reproductive status, or fecundity [see reviews in Bradley & Mundy, 2008; Dixson, 2012, Dubuc et al., 2014; Gerald, 2003]. Skin color may be a particularly sensitive and more honest signal of shortterm health and quality because skin is more immediately inﬂuenced by physiological changes in hormones, hydration, or nutrition [Caro, 2005], as well as mood [Changizi et al., 2006]. Male mandrills have vivid skin color that is status-dependent
© 2015 Wiley Periodicals, Inc.
[Setchell & Dixson, 2001], and reddened males are preferred by females [Setchell, 2005]. A similar phenomenon has been observed in macaque males [Khan et al., 2011]. Not only are color displays important in mate choice, but they may also play an important role in intrasexual competition. Setchell & Dixson  argue that coloration indicates social status among male mandrills. Vervet males assert their dominance over subordinates by presenting their perineal region in a red-white-and-blue display Contract grant sponsor: NSF; contract grant number: BCS0923791; contract grant sponsor: National Evolutionary Synthesis Center (NSF grant); contract grant number: EF-0905606. Conflicts of interest: The authors report no known conflicts of interest.
Correspondence to: James D. Pampush, 1112 Turlington Hall, University of Florida, Gainesville FL, 32611. E-mail: [email protected]
Received 2 July 2014; revised 10 December 2014; revision accepted 10 December 2014 DOI: 10.1002/ajp.22374 Published online XX Month Year in Wiley Online Library (wileyonlinelibrary.com).
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Fig. 1. South African Vervet monkey (Cholorcebus aethiops pygerythrus) giving the ‘red-white-and-blue’ display. Like vervets, many of the Old World monkeys have brightly colored genital skin.
[Henzi, 1985; Struhsaker, 1967], perhaps to avoid or alleviate aggressive encounters [Gerald, 2001]. More recently, female coloration has also been recognized as having signal potential to prospective mates and other group members [e.g., Gerald et al., 2007; Gerald et al., 2009; Setchell et al., 2006]. Clearly, primate skin coloration—and particularly circumperineal skin—is an important signaling apparatus among conspeciﬁcs for many primate taxa. Mammalian skin and pelage coloration has been connected to predation avoidance via camouﬂage [Caro, 2005; Endler, 1978], as well as serving a role in thermoregulation (Gloger’s Rule) [Caro 2005; Gloger 1833]. Other recent studies suggest that environmental factors, such as habitat type, play an important role in the evolution of primate pelage [Kamilar & Bradley, 2011] and facial skin color [Santana et al., 2012; Santana et al., 2013]. Building on earlier observations, Gerald  speculated that in addition to the conspeciﬁc signaling roles and associated sexual selection effects, environmental selective agents likely affect circumperineal coloration. Despite a growing body of literature on how environmental factors impact the evolution of facial skin and pelage coloration among primates (see above), the roles of environmental factors in circumperineal skin color evolution remain underexplored.
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This omission is particularly glaring because the circumperineal skin of many primates is noted for conspicuous reds and blues [e.g., Cramer et al., 2013; Kingdon, 1974], and because circumperineal skin coloration has been so thoroughly studied for its signaling role [e.g., Gerald, 2003; Higham, 2009; also see above]. Camouﬂage is an unlikely explanation for the vividly colored red, blue, and violet circumperineal skin observed in some cercopithecoids. Supporting Gloger’s Rule, Kamilar & Bradley  found that primate pelage is associated with habitat type with species having darker pelage in more dense, tropical habitats. While thermoregulation may have played a role in the evolution of primate pelage patterns and colors, its role in circumperineal color seems unlikely because circumperineal skin represents a relatively small area of the body—unlike pelage which covers most of the body—and because the circumperineal region is not consistently exposed to solar radiation. Alternatively, the evolution of circumperineal coloration may represent a compromise between competing selective pressures. Bradley & Mundy [2008: 109] state (emphasis theirs) “Coloration also reﬂects an interesting tradeoff between the forces of natural selection, which favor camouﬂage and concealment, versus the forces of sexual selection, which favor conspicuous colors signaling quality or availability to prospective mates.” Bradley and Mundy’s  tradeoff observation aligns well with Kingdon’s argument [1974, 1980] that among the cercopithecoids, circumperineal and facial skin coloration is linked with ecology and also serves important visual communication roles between conspeciﬁcs. Kingdon further speculated that terrestrial monkeys are more vulnerable to predation both because they are frequently on the ground, and because they tend to live in more open habitats [Kingdon, 1980]. Under these conditions, Kingdon argued that positioning coloration in the circumperineal region represents an adaptation for avoiding predation while still maintaining the coloration’s utility in intraspeciﬁc communication. This adaptative inference is derived from the observation that circumperineal skin can be opportunistically displayed for intraspeciﬁc communication, via assuming particular postures, and then more easily concealed in avoiding predator detection. As observed by Kingdon  and others [e.g., Bradley & Mundy, 2008], there is an association among Old World monkeys between exhibiting circumperineal skin coloration and terrestrial ecology. Additionally, traditional frequentist statistics conﬁrm this statistically signiﬁcant association between terrestriality and the presence of circumperineal skin coloration (Table I). Among the Cercopithecoidea sampled here, 59 of the 78 species (75%) fall into either the category of uncolored circumperineal regions and arboreal ecology, or colored circumperineal regions and terrestrial
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TABLE I. Distribution of Arboreal/Terrestrial, Uncolored/Colored taxa among extent Old World Monkeys
Uncolored genitals Colored genitals Total
37 7 44
12 22 34
49 29 78
X2(1) ¼ 19.55, P < 0.001, The two-way table here showing the distribution of the species within the four trait-pair conditions. The Arboreal/ Uncolored, and Terrestrial/Colored conditions occur at a greater rate than expected.
ecology (X2(1) ¼ 19.550, P < 0.001). This association has lead some primatologists to speculate on the evolutionary relationship of these two traits, as well as to generate inferences about these traits functions based on their observed association [e.g., Davison, 1982; Kingdon, 1974] though the idea has not been tested [see Prum & Torres, 2004]. While traditional statistics demonstrate a signiﬁcant association between terrestriality and circumperineal coloration among cercopithecoids, this association may not be the direct result of functional association. The assumed functional relationship can be better explored by including information about the phylogenetic relationships among the Old World monkeys. It is important to account for phylogenetic relationships in order to protect against statistical errors arising from species non-independence. Therefore, the purpose of this paper is to explore the association of circumperineal skin color and terrestrial ecology among the Cercopithecoidea with a phylogenetic perspective, and to discuss the evolutionary scenarios which may have generated the observed association. METHODS From the literature, we created a database of 78 cercopithecoid species for which circumperineal color and habitat use information were available [Gerald, 2003; Rowe et al., 2013; Treves, 1997]. Species exhibiting red, blue, or both colors in the circumperineal region were scored as having colored circumperineal skin; species without were scored as uncolored. Species ecology was classiﬁed as either arboreal or terrestrial based on Rowe’s All the World’s Primates database , as well as his other works [Rowe, 1996] (species list and categorical designations available in Fig. 2). In order to effectively test hypotheses involving the coevolution of traits, biologists must consider phylogenetic relationships in their analyses. Fortunately, techniques and accompanying software have been developed which allow researchers to account for this phylogenetically derived nonindependence [see Nunn, 2011 for review]. One such program is BayesTraits [Pagel & Meade,
2006], which offers phylogenetically controlled Bayesian Reversible Jump Markov Chain Monte Carlo (RJ-MCMC) analyses. These analyses can be performed on pairs of discrete traits and are aimed at discerning if their correlated distribution is the product of related evolutionary rates, or the product of incidental coevolution among taxa. An RJ-MCMC analysis was employed using BayesTraits v.2 [Pagel & Meade, 2006]. The chain was sampled every 200 times over 200,100,000 iterations following a burn in of 100,000 iterations for a ﬁnal posterior sample size of 1,000,000. Exponential hyper priors were drawn from a uniform distribution of zero to one. The RJ-MCMC method is advantageous to more conventional MCMC techniques in that it asks the MCMC algorithm to select among competing models in addition to choosing among varying rates, favoring less complex models. In other words, in addition to estimating the size of the transition rates between states, the RJ-MCMC also seeks to simplify the model as much as possible via setting rates equal to one-another, or ﬁxing them at zero (i.e., eliminating evolutionary pathways). The analyses were performed ﬁve times to ensure consistency of the results. Phylogeny was accounted for using a set of 10,000 phylogenetic trees (see Fig. 2 for consensus tree) downloaded from the 10kTrees website (http:// 10ktrees.fas.harvard.edu/) [Arnold et al., 2010]. This block of trees is necessary to account for phylogenetic uncertainty, a problem particularly pervasive among the Asian Colobinae, where there is disagreement over relationships. In addition to testing the evolutionary relationships between the two traits, nodal reconstructions were calculated throughout the phylogeny. To further test that the independent models were not signiﬁcantly worse at predicting modern distribution of these two traits than dependent models, we performed an additional 200,000,000 iteration model restricting the related rate pairs to equality (i.e., independent model) and recovered the posterior harmonic mean for comparison to the dependent models’ posterior harmonic mean. Analyses were performed on the posterior distribution to ensure, effective mixing, and convergence of the model, as well as hypothesis testing. The research presented here conformed to the guidelines of the University of Florida Institutional Care and Use of Animals Committee, as well as conformed to the American Society of Primatologists, guidelines for primate-based research. No actual animals were used in this study. RESULTS The ﬁve RJ-MCMC models appear to have converged, and showed very similar results so for the purposes of space only one is presented here. A
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Fig. 2. Showing the trait pair conditions among the living Cercopithecoidea, as well as internal nodal and root reconstructions based on the posterior distribution of the RJ-MCMC. Note that no-one particular trait pair condition is favored at the root, but there is a quick shift there after at the respective bases of the Cercopithecinae and Colobinae clades.
time series plot of iteration number against harmonic mean shows the tabling of the harmonic mean following the sharp drop indicating the model has reach convergence, and therefore represents a stable sample (Fig. S1). Generally, to ensure adequate mixing of the model, acceptance rates should fall between 20–40% to be certain the parameter space as been sampled thoroughly. The histogram in Figure S2 and the mean (0.28), median (0.27), and mode (0.24) acceptance rates indicate the RJ-MCMC performed adequately. Time series plot of loglikelihood values against iteration number for the posterior distribution of the model demonstrate the ‘woolly bugger’ appearance which is further indication that the model has effectively sampled the parameter space without becoming trapped in areas of especially unusual likelihood which may lead to autocorrelation in the posterior distribution (i.e., a lack of autocorrelation is shown in Fig. S3). The frequency distribution of log-likelihood values for the posterior distribution of the model demonstrates the negative skew common to converged, well mixed, analyses (Fig. S4). Taken together, Figures S1–S4 indicate that the model mixed sufﬁciently and converged, therefore the results from this analysis can be interpreted with conﬁdence, the posterior distribution was analyzed for hypothesis testing.
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The BayesTraits program controls for phylogeny by estimating and comparing rates of change along branch lengths for two separate traits. If the two traits are adaptively related—and assuming no pleiotropic effects—then the background condition of one trait, should impact the transition rate of the other (dependent model). This will be reﬂected in the rate values (q-values which are time scaled proportional values; for greater explanation of q-values see Pagel ) provided in the RJ-MCMC’s posterior distribution. For example (refer to Fig. 3), if terrestrial ecology promotes evolution of circumperineal coloration among the Cercopithecoidea, then we would expect the rate q34 (transition from condition 3 i.e., terrestrial-uncolored to condition 4 i.e., terrestrial-colored) to be greater than the rate q12 (transition from arboreal-uncolored to arborealcolored). If rates q12 and q34 are equal, this then indicates that species that are terrestrial are not more likely to develop circumperineal coloration (i.e., independent evolution of the traits). Indeed if the two traits are evolutionarily related, then we would expect most of the rates pairs (q12 & q34; q24 & q13, q43 & q21, and q31 & q42) to be unequal. As stated above, one of the advantages of the RJ-MCMC algorithm is that it will choose among competing models, not just among competing rates within one
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Fig. 3. Flow-diagram for transition rates between discrete traitpair conditions. Values behind q are code for transition between condition categories (i.e., q12 indicates transition rate between condition 1 to condition 2). Comparisons of q12 & 34, q24 & q13, q43 & q21, and q31 & q42 reveal whether or not the background condition for one trait impacts the transition rate of the other trait. Comparisons of the rate pairs in this study do not indicate that Arboreality vs Terrestriality is related to the presence of circumperineal coloration.
particular model. Table II shows the ten most common models in the posterior distribution. These models only account for 23.9% of the entire posterior distribution and among them only model 10 is signiﬁcantly worse than any of the other models (log-likelihood test, P ¼ 0.004). Compare these values to Pagel and Meade’s  demonstration of this technique in which their RJ-MCMC’s 10 most common models accounted for 50% of all model visits, and the two most common accounted for nearly 24% of their posterior distribution. In other words, while the models presented in Table II are the best models according to the Bayesian RJ-MCMC analysis performed here, collectively they account for a small portion of the posterior distribution, indicating low conﬁdence in ﬁnding a single model or a group of related models to explain the co-evolution of these traits. This is further demonstrated in that, no one particular model among the nine most common
stands out. Furthermore, among the four rate pairs, only one—q13 & q24—is consistently unequal among the nine most frequent models, with rate q24 favored for a slightly higher rate. Additionally, a binomial test indicates that paired rate inequality occurs basically at random (Table III). At best, these frequency results indicate very weak interaction between these two traits. When comparing the relative number of times the sampling chain visited independent vs. dependent models, neither model type was visited signiﬁcantly more often than expected (Table IV). The values presented in Table IV can be a bit misleading because as can be seen in Table V, while there are over 21,000 different possible models to sample from, only 51 (0.2%) of those models are of independent evolution of the two traits. The RJ-MCMC visited independent models 1,337 times in our sample of 1,000,000 but was anticipated to visit independent models 2,400 times by chance. The Bayes factor value testing the correlated evolution of these traits (calculated as the posterior odds/prior odds) is one (Table IV). The general rule of thumb for evaluating Bayes factors is values under 3 are considered no support for the model, in this case, no support for the dependent evolution of the two traits. Values between 3 and 10 are considered evidential of the model, values between 10 and 100 are strong evidence, and values greater than 100 are considered decisive [Jeffreys, 1967]. In other words, the analyses performed here do not give good reason to believe that terrestrial ecology and circumperineal coloration co-evolved as part of some trait complex in cercopithecoids since models of dependent trait evolution are not signiﬁcantly better than independent models. For a more complete discussion on calculating Bayes factors from posterior and prior probabilities see Currie et al.,  and/or Pagel& Meade, . Lastly, after restricting the model rates to equality (i.e., independent model) harmonic means
TABLE II. Top 10 Most Frequently Visited Models of Trait Evolution Model 1 2 3 4 5 6 7 8 9 10
Z Z 0 0 1 1 Z 0 Z Z
0 0 0 0 1 1 0 0 1 0
0 Z 0 0 1 1 Z 1 Z 0
1 1 1 1 0 0 1 1 0 0
1 1 1 1 0 0 1 1 0 0
1 0 0 Z 1 1 1 1 1 0
1 1 1 1 1 0 1 1 0 0
0 0 0 0 1 1 0 0 1 Z
32,229 31,696 30,199 27,119 26,022 24,157 21,700 19,786 18,815 18,130
78.287 79.433 78.752 78.815 79.344 79.746 79.993 78.708 79.450 83.735
3.2% 3.1% 3.0% 2.7% 2.6% 2.4% 2.2% 2.0% 1.9% 1.8%
3.2% 6.3% 9.3% 12.0% 14.6% 17.0% 19.2% 21.2% 22.1% 23.9%
Table showing the 10 most frequently visited models in the posterior distribution of the RJ-MCMC. The algorithm visits models in proportion to their loglikelihood. PDF ¼ Probability Density Function, calculated as number of observations/1,000,000 (number of iterations sampled). CDF ¼ Cumulative Density Function, the summation of the models in sequence of frequency.
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TABLE III. Paired Rate Equality Among 10 Most Common Models Paired rates equal
Paired rates unequal
Table showing the number of occurrences of paired rate equality and inequality among the 10 most frequent models in the posterior distribution. A binomial test indicates that paired rate equality/inequality occurs at random. This is further demonstration that terrestriality and circumperineal coloration did not functionally co-evolve among cercopithecoids.
for an independent model were recovered and compared to the harmonic means of the dependent models. Log-likelihood ratio tests indicate that dependent models are not signiﬁcantly better than independent models (P ¼ 0.396, Table IV). DISCUSSION Using a phylogenetic RJ-MCMC approach, we found that within the cercopithecoid clade (using the available data), evolutionary rate models indicate that the shift toward circumperineal coloration is not affected by the background condition of terrestriality (nor vise-versa). Among the Cercopithecoidea sampled here, most of the species with circumperineal color are also terrestrial and most of the species without circumperineal color are arboreal. Although this may seem to suggest that these features are part of some functional trait complex, our Bayesian rate analyses found that these two traits appear to have evolved independently rather than as part of a particular trait complex. What follows is a discussion of the potential phenomena we believe we have observed from conducting this analysis. Potential Statistical Errors and the Need for Phylogenetic Perspective An interesting ﬁnding of this research is demonstrated by the discordance of conclusions drawn from the traditional frequentist statistical approach, and the rates-based Bayesian method developed by Pagel
& Meade . As demonstrated in Table I, a frequency distribution X2 analysis shows there to be a signiﬁcant association between terrestrial ecology and circumperineal coloration among the Old World monkeys (and mirrored in arboreality and lack of circumperineal coloration). This observation may have lead Kingdon [1974, 1980] to propose a functional relationship between these two traits, centered on the idea that locating a conspicuous intra-speciﬁc signaling mechanism in the circumperineal region represents an adaptation to avoiding predator detection. Bradley & Mundy  would likely interpret this as an adaptive solution to the cross-purpose actions of natural and sexual selection. From this, an interesting—but speculative—evolutionary narrative can be constructed which goes as follows: in the past among certain ancestors to Old World monkeys, coloration of skin became an important sexual signaling mechanism (it does not matter whether it be between members of the same or opposite sex). As these same taxa—or their descendents—began to explore terrestrial habitats (as with early members of the Victoriapithecidae [Blue et al., 2006]) greater terrestriality may have exposed these taxa to more predation pressure. To deal with the conspicuous nature of their sexual signaling apparatus in a new (potentially) predator rich environment, the Old World monkey lineages may have adaptively relocated their colored skin to their circumperineal regions, which enabled them to conceal it when necessary. An alternative narrative can be constructed in which terrestriality takes primacy, and a return to an arboreal environment reduces the need for coloration located in the circumperineal region. There are several things that make the Bayesian-based method of Pagel & Meade  different from the frequentist X2 test used as evidence for the narrative above, but most important among them in generating the observed discordance is the measures being used for hypothesis testing. The Pagel & Meade  method is comparing modeled rates of evolutionary transitions, not the distribution of taxa into discrete categories. While the X2 test essentially asks if the distribution of taxa into categories is even (null hypothesis) or not
TABLE IV. Independent vs Dependent Model Frequencies and Log-Likelihoods
Independent models Dependent models
0.24% 2400 99.76% 997601
log-likelihood test P-value 0.396
Table shows the frequency of independent and dependent models in the posterior distribution of the RJ-MCMC. Independent models are far less common due to the rate-pair restriction requirements and only 51 different models are possible for an eight-parameter model. Bayes factor calculated as posterior probability/prior probability. Value of 1 indicates models are sampled at approximately the rate expected by chance. Log-likelihood calculated as -2(loglikelihood dependent model—log-likelihood independent model). P-value calculated from X2 distribution with 1 degree of freedom.
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TABLE V. Number of Possible Models Binomial for Number Binomial Bell number Z * Bell of Zeros (Z) for Z 8-Z for 8-Z Number for 8-Z 0 1 2 3 4 5 6 7 8
1 8 8 7 28 6 56 5 70 4 56 3 28 2 8 1 1 0 Total Number of
4,140 877 203 52 15 5 2 1 0 Models:
4,140 7,016 5,684 2,912 1,050 280 56 8 0 21,146
Calculation table for the total number of different models possible in an eight-parameter model. The total number of models is needed to calculate Bayes Factors in testing independent vs. dependent evolution hypotheses in this analysis.
(alternative hypothesis). The method used in the results presented here asks if the likelihood of evolutionary transition from uncolored to colored circumperineal skin (or vice-versa) is related to terrestrial ecology in Old World monkeys. If it were the case that these two trait categories were functionally related (alternative hypothesis), then we would expect the background condition of one trait to inﬂuence the evolutionary transition rate of the other trait—which was not found in this study. A central part of measuring evolutionary transition rates rather than the patterning of trait distribution using the Pagel & Meade  method, is the incorporation of phylogenetic relationships into the analyses. So while reconstructing the evolutionary transition rates between discrete character states is the proximate goal of the approach, it has the ultimate effect of controlling for phylogenetic relationships (although, to be fair, Pagel & Meade  designed their technique explicitly to control for phylogeny). Felsenstein  and others [e.g., Grafen 1989; Orme et al., 2012; Stone et al., 2011] have pointed out the statistical problems associated with not controlling for phylogeny, in particular, the increase of both type I (false positive) and type II (false negative) errors due to species non-independence. Reconstructing the transition rates between character states here has potentially identiﬁed the X2 results to be a type I error —in terms of the interacting relationship between circumperineal skin coloration and terrestriality. Therefore, the discordance of these results from different approaches underscores the need to control for phylogeny when making any multispecies (more than 2) comparative analysis of traits. Limitations of the Model The model (or set of models in the posterior distribution) presented is a broad simpliﬁcation of
the actual animals and—more importantly—the evolutionary process which produced the extant array of Old World monkey features. The BayesTraits v.2 program [Pagel & Meade, 2006] requires a simpliﬁcation of the biology for the taxa being investigated. Many of the cercopithecoids are probably not best described as simply ‘arboreal’ or ‘terrestrial’ and a semi-terrestrial category would more accurately describe some of the monkeys. Indeed, Rowe and others [Rowe, 1996; Rowe et al., 2013] categorized some of the taxa used in this study as semi-terrestrial, but in order to engage the problem using the technique presented here, simplifying assumptions about the monkeys’ ecologies are needed. To that end, monkeys classed as semi-arboreal were categorized as terrestrial in this study, with the rationale being that based on Kingdon’s hypothesis [1974; 1980] terrestrial behaviours expose Old World monkeys to greater predation pressure. The additional simpliﬁcation of the color signaling mechanisms (both red and blue) into a single binary trait as present or absent ignores the complexity of the evolution of these characters. Some researchers have argued that blue coloration in primates has evolved at least twice [Prum & Torres, 2004], and the reddened skin signals at least twice as well [Caro, 2005] in Old World monkeys. However, there are several consistencies in these circumperineal signals—regardless of the physical mechanisms producing them—such as their roles in intra-speciﬁc communication, the conspicuousness of the colors, and their anatomical location. Ultimately, the model presented here is a heuristic attempt to understand the relationship between terrestrial ecology and circumperineal coloration among Old World monkeys. The observed pattern (see Table I, Fig. 2) can only be appreciated on a clade-wide scale, and a modeled analysis of that pattern will require broad simpliﬁcations. Potential Causes of the Current Trait Association There are several competing hypotheses which may explain why the majority of Old World monkeys show either colored circumperineal regions with terrestrial ecology, or uncolored circumperineal regions with a more arboreal ecology. Examining the ancestral state reconstructions—granted there tends to be a high degree of uncertainty associated with these kinds of results—can provide some tentative insights into how these characters coevolved. Reconstructions at the root of the phylogeny (last common ancestor of extant Cercopithecoidea) are: 21.7% Arboreal Uncolored, 24.7% Arboreal Colored, 26.1% Terrestrial Uncolored, 27.5% Terrestrial Colored (Fig. 4). That is, the Bayesian reconstructions of the root condition are nearly evenly distributed between the four paired-character states.
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Fig. 4. Pie charts for the nodal reconstructions of the Root of the phylogeny (Ancestral to Cercopithecoidae). Root of the Cercopithecinae clade, and the root of the Colobinae clade. Notice that a majority of reconstructions place the Colobinae last common ancestor as being arboreal and uncolored, while a majority of the reconstructions place Cercopithecinae as being terrestrial and colored.
However, there is a dramatic shift immediately following the split between the two major Old World monkey clades (Cercopithecinae and Colobinae). Bayesian reconstructions at the base of Cercopithecinae estimate: 2.0% Arboreal Uncolored, 10.2% Terrestrial Uncolored, 36.5% Arboreal Colored, and 51.3% Terrestrial Colored (Fig. 4). Over 50% of the time, the root of the Cercopithecinae is reconstructed as possessing colored circumperineal skin and terrestrial ecology. When examining the Bayesian reconstructions at the base of the Colobinae show a similar—but reversed—distribution is observed: 4.1% Terrestrial Colored, 8.3% Arboreal Colored, 32.1% Terrestrial Uncolored, and 55.5% Arboreal Uncolored (Fig. 4). The nodal reconstructions are further conﬁrmed by a X2 analysis looking at the
distribution of the traits in relation to their subfamily (Cercopithecinae vs. Colobinae) afﬁliations. Subfamily afﬁliation is a statistically signiﬁcant predictor of the distribution of character states (P < 0.001, P < 0.001, respectively, Table VI). First, considering these results together, the modern distribution of traits may be a consequence of selective pressure functionally pairing these traits together according Kingdon’s [1974; 1980] proposal during the colobine-cercopithecine cladogenic event, followed by some form of stabilizing selection—as has been demonstrated or argued in other works [e.g., Revell et al., 2008; Wiens & Graham, 2005]. Parsimony analysis of the number of transitions between the states shows that there were a minimum of 14 transitions between arboreal and terrestrial (or vice-versa) and a minimum of 11 transitions between colored and uncolored circumperineal regions (or vice-versa). This relatively small number considering the 78 taxa and 77 internal nodes may be an indication that the traits do not evolve very rapidly, and thus are under some kind of stabilizing selection, although importantly, these values represent transitions minima, there were likely more than just 25 total transitions between the traits within the clade. Regardless, the Bayesian rate analyses did not reconstruct those 25 transitions to be coordinated, so perhaps this indicates a relatively relaxed stabilizing selection pressure, or one which relaxed through time. Secondly, the discordance in the results (between the X2 and BayesTraits), and the non-coordinated evolution of the two traits may be the result of phenomena occurring at the genetic level. The two traits may be genetically linked via pleiotropy [Blomberg & Garland, 2002; Kamilar & Cooper, 2013; Wiens & Graham, 2005]. That is, the gene or gene complex associated or controlling for circumperineal coloration may also inﬂuence the proclivity
TABLE VI. Two-Way Tables for Trait Distributions Phylogeny-based distribution tests Ecology Distribution Arboreal Terrestrial Total Coloration distribution Uncolored Colored Total
Colobinae 26 3 29 Colobinae 26 3 29
Cercopithecinae 23 26 49 Cercopithecinae 18 31 49
Total 49 29 78 Total 44 34 78
X2 X2(1) ¼ 14.23 P < 0.001 X2 X2(1) ¼ 20.75 P < 0.001
Two-way table chi-square analyses show likelihood of the trait-pair distributions. Root and nodal reconstruction values calculated from the RJ-MCMC assigning ancestral values to nodes and the root in the phylogeny. Tests on those nodal and root reconstructions indicate that the pairing of colored genital with terrestriality, and uncolored genitals with arboreality do not occur at higher rates than would be expected by chance. The Phylogeny based distribution tests however, indicate that the number of arboreal Colobinae are higher than expected given the full distribution of the trait among the Cercopithecoidea. Additionally, the distribution of colored genitals is unusual with Colobinae showing a much lower number of species, and the Cercopithecinae showing a much higher number of species than would be predicted by chance.
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towards terrestriality in Old World monkeys (or arboreality with uncolored circumperineals). The distribution of the traits throughout the phylogeny may represent an initial genetic association of the two traits followed by decoupling within certain lineages producing both the observed pattern in modern taxa, and the lack of coordinated evolution found in the rates analyses. Some studies have found tentative genetic links between morphological traits and behavioral traits [e.g., Trut et al., 2006]. Alternatively, one or both of the traits may evolve sluggishly not just from stabilizing selection—as suggested above—but due to a lack of genetic variation produced from either:  intrinsic genetic constraints,  gene ﬂow constraining variability, or  stabilizing selection on some unmeasured trait which is pleiotropically integrated with circumperineal coloration or terrestrial proclivity. Lastly, the modern distribution of character states at the tips of the Old World monkey phylogeny may be the product of historical contingency dating back to the initial subfamily cladogenesis event. This ﬁnal explanation also ﬁts with the modeled rate parameters which clearly indicate that the background condition for one trait does not impact the likelihood of transitioning between states for the other trait. Many evolutionary biologists may ﬁnd this conclusion to be unsatisfactory or unproductive. Gould [2002: 1338] captured this disaffection best when he wrote: “we tend to begin with a preference for explanation by predictability and subsumption under spatiotemporally invariant laws of nature, and to move towards contingency only when we fail. Contingency therefore becomes a residual domain for details left unexplained by general laws.” This last explanation is also drawn on the failure to connect—through evolutionary rates—circumperineal skin coloration with terrestriality. If the cladogenetic event which produced the separate colobine and cercopithecine clades were to be ‘replayed’ and because the model presented here shows no evidence of an adaptive association between the character states of terrestrial/arboreal ecology and colored/uncolored circumperineal skin, then any combination of the trait states seems equally likely for the bases of the subfamilies, unless it can be shown that one of the above explanations is valid. While extremely difﬁcult to prove within the framework of the current positivist scientiﬁc paradigm, historical contingency is theoretically highly likely to have had signiﬁcant effects on current biological forms because of the tinkering and historical nature of the evolutionary process [Gould, 1991; Gould, 2002; Harms & Thornton, 2014]. Terrestriality and Primate Predation Pressure Arguments for the functional association of circumperineal coloration and terrestriality have
viewed predation pressure as a strong selective force in these traits’ coevolution. The magnitude and therefore the role of predation pressure on primate groups has been a large source of debate, with some arguing it has minimal evolutionary/ecological impact on primates [e.g., Cheney & Wrangham, 1987; Dunbar, 1988; Wrangham, 1980], while others view it as perhaps the most important ecological variable [e.g., Terborgh & Janson, 1986; van Schaik, 1983]. Much of this debate likely stems from the difﬁculty in quantifying, or qualifying, primate predation pressure [for review see Enstam, 2007]. Regardless of the level of selection pressure predation applies to primates, primatologists have traditionally inferred that terrestrial primates were at greater predation risk than arboreal taxa [e.g., Dunbar, 1988; Plavcan and van Schaik, 1994]. This traditional inference is a cornerstone of Kingdon’s [1974, 1980] adaptive hypothesis regarding locating color signals in the circumperineal region for high-predation-risk primates (i.e., terrestrial primates). Predation pressure has apparently played an important role in the evolution of plumage coloration in birds [Zink & Remsen, 1986] and has been hypothesized to play an important role in skin and pelage coloration among primates [Kamilar & Bradley, 2011; Santana et al., 2013]. However, while predation has likely played an important role in many aspects of cercopithecoid evolution (including pelage adaptations), there are several reasons to conclude that it has not affected the pairing of circumperineal skin coloration and terrestriality. First, the model presented in this research does not support a functional relationship between circumperineal skin coloration and terrestriality. Second, considering the visual system of predators is important in understanding how predation pressure may impact the visual appearance of primates. For cercopithecoids, key predators include snakes, raptors, and carnivores, but especially felids throughout Africa and Asia [Anderson, 1986; Hart, 2007]. Physiological experiments on felids indicate they have only two types of cone photoreceptors and thus do not see a full catarrhine-primate color ﬁeld [Jacobs, 1993; Jacobs & Nathans, 2009]. In particular, Jacobs  suggests that felids cannot distinguish reds and greens. Therefore, bright red coloration, regardless of its location, is unlikely to attract a felid predator’s attention. Birds of prey on the other hand, have full color vision and color signals would likely attract their attention [Ödeen & Håstad, 2003]. Lastly, a metaanalysis by Hart  compiling global records on primate predation has shown that in Africa and Asia, terrestrial cercopithecoid primates are not under signiﬁcantly greater predation pressure than their arboreal cousins. Hart  acknowledges the differing perceptions on the importance of predation pressure among primatological researchers, but clearly demonstrates that regardless of the overall
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magnitude of the selective pressure exerted by predation, terrestrial primates are not at higher risk than arboreal ones. Further, Shattuck & Williams  argue that terrestrial primates have a number of adaptations for ameliorating predation pressure, and likely experience it at the same rate (because of the anti-predation adaptations) as their arboreal cousins. CONCLUSION Rates-based analyses on the co-evolution of circumperineal skin coloration and terrestriality among Old World Monkeys failed to show correlated evolution of the traits though there is a statistically signiﬁcant association in modern taxa. This could be the result of several different evolutionary phenomena including: stabilizing selection after the cercopithecine-colobine cladogenesis event, pleiotropic gene effects, intrinsic/ extrinsic genetic constraints, or historical contingency. The results of this paper underscore the need to consider both phylogenetic relationships in statistical analyses of modern traits, and developing methods or investigations capable of indentifying a particular evolutionary process among those capable of generating similar evolutionary patterns. ACKNOWLEDGEMENTS The authors would like to thank the many people who helped make this manuscript possible including but not limited to: Dr. David Daegling, Susan E. Lad, and Kim N. Le who read earlier versions of this manuscript. Additional thanks to Dr. John Krigbaum, Paul Morse, and Dr. Karen Bales and three anonymous reviewers. For assistance with the phylogenetic techniques used in this paper, thanks to the AnthroTree Workshop funded by NSF (BCS0923791) and the National Evolutionary Synthesis Center (NSF grant EF-0905606) and its helpful instructors, especially Dr. Charlie Nunn and Dr. Thomas Currie. Two anonymous reviewers’ comments dramatically improved this manuscript.
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