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. Author manuscript; available in PMC: 2020 Nov 1.
Published in final edited form as: J Comp Psychol. 2019 Jun 27;133(4):512–519. doi: 10.1037/com0000183

Further Evidence of a Left Hemisphere Specialization and Genetic Basis for Tool Use Skill in Chimpanzees (Pan troglodytes): Reproducibility in Two Genetically Isolated Populations of Apes

William D Hopkins 1,2,+, Mary Catherine Mareno 1, Steven J Schapiro 1,3
PMCID: PMC6813849  NIHMSID: NIHMS1025243  PMID: 31246047

Abstract

It has been hypothesized that the evolution of tool use may have served as a preadaptation for the emergence of left hemispheric specialization in motor skill in humans. Here, we tested for intermanual differences in performance on a tool use task in a sample of 199 captive chimpanzees in relation to sex, age and their hand preference. Additionally, we examined heritability in tool use skill for the entire sample, as well as within two genetically isolated populations of captive chimpanzees. This was done to determine the degree of reproducibility in heritability on motor performance. The results revealed a significant effect of hand preference on intermanual differences in performance. Right-handed chimpanzees performed the task more quickly with their right compared to left hand. In contrast, no significant intermanual differences in performance were found in left- and ambiguously-handed apes. Tool use performance was found to be significantly heritable for overall performance, as well as separately for the left and right hands. Further, significant heritability in tool use performance was found in both populations of apes, suggesting these results were reproducible. The results are discussed in the context of evolutionary theories of handedness and hemispheric specialization and the genetic mechanisms that underlie their expression in primates, including humans.

Keywords: Hand skill, manual asymmetry, heritability, chimpanzees, tool use

Humans show a left hemisphere specialization for praxic functions. Notably, cross-cultural studies have shown a statistical majority of humans self-report preferring their right hand for use in a number of manual actions (Perelle & Ehrman, 1994; Porac & Coren, 1981), including data from non-Westernized societies (Marchant, McGrew, & Eibl-Eibesfeldt, 1995; Raymond & Pontier, 2004). Besides preferring their right hand, most humans also perform simple motor actions better with their preferred compared to non-preferred hand (Brown, Roy, Rohr, Snider, & Bryden, 2004; Bryden, Mason, & Gonzalez, 2016; Corey, Hurley, & Foundas, 2001; Dellatos et al., 2003; Doyen, Dufour, Caroff, Cherfouh, & Carlier, 2008; Nelson, Berthier, & Konidaris, 2017; Peters & Ivanoff, 1999; Steenhuis & Bryden, 1999; Tapley & Bryden, 1985). In light of the fact that most individuals prefer to use their right hand, not surprisingly, the right hand performs better than the left on tasks that assess motor skill and strength; however, and critically, the degree, and pattern, of asymmetry observed in manual skill performance are fundamentally different from hand preference data.

Whether nonhuman animals, and specifically, nonhuman primates exhibit left hemisphere specialization in manual motor function remains a topic of intense historic and contemporary scientific interest and debate (Cashmore, Uomini, & Chapelain, 2008; M. C. Corballis, Badzakova-Trajkov, & Haberling, 2012; Crow, 2004; Fagot & Vauclair, 1991; Forrester, Quaresmini, Leavens, Mareschal, & Thomas, 2013; Hopkins, 2006; MacNeilage, Rogers, & Vallortigara, 2009; Marchant & McGrew, 1991; McGrew & Marchant, 1993, 1996; L. J. Rogers & Andrew, 2002; Vallortigara & Bisazza, 2002; J. M. Warren, 1980). There has been a plethora of studies across a wide range of nonhuman primate species examining whether monkeys and apes show population-level hand preferences, and the collective findings have produced somewhat mixed results (Meguerditchian, Vauclair, & Hopkins, 2013; Strockens, Gunturkun, & Sebastian, 2013). In contrast to humans, far fewer studies have considered performance asymmetries in manual skill rather than hand preferences, which are arguably much more prone to the influence of situational and other non-biological factors (Hopkins, 2018).

In this study, new data on performance asymmetries and heritability in motor skill in captive chimpanzees are presented, building on previous findings in chimpanzees. Specifically, Hopkins, Russell, Schaeffer, Gardner, and Schapiro (2009) measured hand preference and skill in captive chimpanzees for a simulated termite fishing task, recording the hand used and the latency to successfully insert a stick into a small hole for 50 responses. Hopkins et al. (2009) found that chimpanzees failed to a show a population-level asymmetry in hand preference and hand skill when intermanual differences in latency were compared between the left and right hands. Hopkins et al. (2009) further reported mean latency in dipping responses were significantly faster for the dominant compared to non-dominant hand, findings consistent with a recent report in wild chimpanzees (Sanz, Morgan, & Hopkins, 2016). One limitation of the Hopkins et al. (2009) and Sanz et al. (2016) studies, particularly as it relates to tool use skill for the dominant and non-dominant hand, was a lack of control for the number of responses for each hand. Specifically, in Hopkins et al. (2009), the chimpanzees could use either their left or right hand during each of the 50 responses. Thus, when comparing the latency data between the left and right hands, an unequal number of responses were made by the left and right hands, which may have biased or skewed the performance data for each hand. To address this limitation, in this study, as in Hopkins et al. (2009), measures of latency in responding on a tool use task were recorded, but we obtained exactly 30 responses for both the left and right hands in samples of left-, ambiguously- and right-handed chimpanzees. Thus, there were an equal number of responses for each hand allowing for a more accurate and controlled manner of testing for intermanual differences in motor skill in the chimpanzees.

In addition to the measurement of performance asymmetries, we also tested for heritability in tool use latency. Hopkins, Reamer, Mareno, and Schapiro (2015) previously found that overall tool skill (averaged across all responses) was significantly heritable in chimpanzees. However, Hopkins et al. (2015) did not test for heritability in latency for each hand because, as noted above, there were an unequal number of responses. By collecting an equal number of responses for each hand in this study, we were able to test for heritability in overall latency, as well as for the latency of each hand as a means of assessing whether one hemisphere may or may not be more strongly implicated in the potential genetic basis for motor skill.

Lastly, we tested for reproducibility in both the behavioral and heritability results among the chimpanzees. Recently, much has been written regarding the increased need for replication and reproducibility in the social and biological sciences (Baker, 2016; Collaboration, 2015). Here, we took advantage of the demographics of the US captive chimpanzee population to test for the reproducibility of the data obtained in this study. Notably, we tested tool use latency and performance asymmetries in two genetically isolated populations of chimpanzees. Each chimpanzee population was developed from distinct founder animals and no interbreeding has taken place across facilities. Thus, though they are the same species, they were genetically isolated from each other, providing a unique circumstance for assessing repeatability and reproducibility of the findings, particularly as they relate to heritability estimates in tool use skill.

Method

Subjects

Performance asymmetry and latency data were obtained from 206 captive adult or adolescent chimpanzees including 129 females and 77 males ranging in age from 6 to 53 years. Eight-three chimpanzees were housed at the Yerkes National Primate Research Center (YNPRC) and 123 were living at the National Center for Chimpanzee Care (NCCC) of The University of Texas MD Anderson Cancer Center. All of the subjects in this study were part of the Hopkins et al. (2009, 2015) reports and therefore their hand preference on the tool use task had been previously assessed, and included 67 left-handed, 68 ambiguously-handed (i.e., they had no significant hand preference) and 71 right-handed chimpanzees.

Behavioral Data Collection

Hand preference data were taken from the previous published study by Hopkins et al. (2009). Briefly, the motor and cognitive demands of termite fishing were simulated by using threaded poly-vinyl-chloride (PVC) pipes (approx. 4 cm in diameter and approx. 20 cm in length) attached to threaded (PVC) bases that were affixed to the subjects’ home enclosures at multiple locations approximately 60 to 80 cm above the ground or floor. The pipes were fitted with a disc in one end with a 7 mm hole cut out to greatly reduce the size of the opening available for tool insertion, thus increasing the motor demands of the task. The other end was closed with a removable screw-on cap. The pipes were filled with a preferred food substance that would adhere to the tool, such as mustard, yogurt, syrup, or applesauce, before being screwed into the bases. The chimpanzees were provided with flexible, thin ‘lollipop’ sticks (approx. 11 cm in length and 4 mm in diameter, like those used to make large lollipops), made out of tightly rolled, thin paper. The animals used the lollipop sticks to dip into the small hole of the pipe and retrieve the food, thereby simulating the actions of termite fishing observed in the wild.

Procedure

Each subject was tested on dipping performance for 30 insertions each of the lollipop stick into the device using the left and right hand. Each PVC pipe was filled with a preferred food substance and then screwed onto a base. After placing the device on the enclosure, each subject was supplied with a tool by either handing it to them directly or by dropping it near them. If the tool became unusable, a new tool was offered to the subject. To encourage use of both the left and right hands, the device was positioned at lateral ends of the left and right portion of the home enclosure adjacent to the wall. The sessions were videotaped and subsequently the experimenter recorded the time required to insert the stick into the hole during each successful probe. Time per dip was measured from the time the subject initiated an attempt to insert the tool with one hand and ended when the chimpanzee successfully inserted and removed the tool. If subjects stopped attempting to use the tool, or switched the tool to their mouth or other hand within a dipping bout, the response was not counted.

For each chimpanzee, we calculated the average latency for the 30 responses performed by each hand. We also computed a performance asymmetry quotient (PAQ) following the formula [PAQ = (L – R)/ (R + L)] where R and L represented the mean latency in dipping responses for the right and left hands, respectively. Positive PAQ values reflected faster performance by the right compared to left hand. Negative PAQ values indicated faster performance by the left compared to right hand. Based on the sign of their PAQ score, subjects were classified as performing faster with their left (PAQ_L <= 0) or right (PAQ_R > 0) hand.

Quantitative Genetic Analysis

Total additive genetic variance (h2) is the proportion of total phenotypic variance that is attributable to all genetic sources. Total phenotypic variance is constrained to a value of 1; therefore, all non-genetic contributions to the phenotype are equal to 1 - h2. Many of the chimpanzees in each colony are related and this allowed for an analysis of heritability using quantitative genetics based on the entire pedigree. The software program SOLAR was used to estimate heritability in tool use performance (Almasy & Blangero, 1998). SOLAR uses a variance components approach to estimate the polygenic component of variance when considering the entire pedigree (see Fears et al., 2009; Fears et al., 2011; J.Rogers et al., 2007). SOLAR was used in two ways in this study. First, it was used to estimate and statistically determine whether tool use performance was significantly heritable in the entire chimpanzee sample, as well as within the NCCC and YNPRC populations. Second, we used SOLAR to perform a genetic correlation analysis between the performance measures for the left and right hands. Genetic correlations (RhoG) reflect additive genetic variance that is shared between two traits. That is, it is the extent to which common genetic mechanisms explain two or more phenotypic traits. For all quantitative genetic analyses on the overall sample, colony, sex, age and rearing history of the apes were included as covariates.

Results

Behavioral Data

For the average latency scores, we performed a mixed model analysis of covariance with hand (left, right) as the within-subject factor, while sex (male, female), colony (NCCC, YNPRC) and hand preference (left-, ambiguously- or right-handed) were the between-group factors. Age was the covariate. We found a significant two-way interaction between hand preference and hand use F(2, 193)=9.115, p = .001, ηp2 = 085. (Figure 1a). Post-hoc analysis using a paired t-test indicated that the mean latencies between the left and right hands were not significantly different for left- t(66)=−0.967, p = .337, d = .118 and ambiguously-handed chimpanzees t(67)=−0.460, p = .647, d = .044; however, in right-handed chimpanzees, mean latencies for the right hand were significantly shorter than the left hand t(70)=+3.975, p = .001, d = .470. Age was also a significant covariate F(1, 193)=9.156, p = .024, ηp2 = 045. As a secondary analysis of the age effect, we subsequently performed a partial correlation analysis between the mean latency values and age, while controlling for sex and colony. The partial r value was positive and significant (partial r = .171, p = .014) indicating that older subjects had longer latency values. As an alternative means of examining association between hand preference and performance, we performed a chi-square test of independence between the chimpanzees’ hand preference and PAQ score classification (see Figure 1b) and found a significant association between the two variables X2 (2, N =204) = 12.166, p = .002. As can be seen in Figure 1b, 75% of the chimpanzees that preferred their right hand performed faster with their right compared to left hand. In contrast, among chimpanzees that preferred their left hand, only 54% performed faster with their left compared to right hand.

Figure 1:

Figure 1:

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a) Mean latency (+/− 95% CI) for the left and right hands on the tool use task for left-handed, ambiguously-handed, and right-handed chimpanzees b) Number of individual chimpanzees that performed better with their left ( L < R) or right hand (R < L) in left-handed, ambiguously- and right-handed chimpanzees.

Heritability

The results of the heritability analyses can be found in Table 1. For the overall, NCCC and YNPRC samples, significant heritability was found in mean latency responses, as well as average latency responses for the left and right hands separately. We failed to find evidence of significant heritability for asymmetries in tool use skill for the entire sample or within the NCCC or YNPRC populations of chimpanzees. With respect to covariates, we found that sex, age and hand preference accounted for a significant proportion of variance in overall mean latency and the latency scores for each hand; however, these results were not reproducible between the NCCC and YNPRC samples. In contrast, for asymmetries in latency, we found that subjects’ hand preference was a significant covariate for the entire sample, as well as within both the NCCC and YNPRC populations. These findings are consistent with the previously described behavioral results demonstrating that hand preference was associated with intermanual differences in latency. Finally, again using SOLAR, we performed a genetic correlation between the latency performance data for the left and right hands and found significant genetic (rhoG = .982, se = .108, p = .002) and environmental (rhoE = .491, se = .129, p = .019) associations. Thus, both common genetic and non-genetic factors underlie the expression of the latency data for the left and right hands.

Table 1.

Heritability in Tool Use Performance and Asymmetries

h2 se p Covariates Variance
Entire Sample
Overall Mean .544 .156 .0001 Age, Handedness .045
Right Hand .625 .148 .000009 Age, Sex .043
Left Hand .344 .164 .011 Age, Handedness .089
Asymmetry .172 .133 .071 Age, Sex Handedness .088
YNPRC
Overall Mean .621 .213 .002 Age, Sex, Handedness .098
Right Hand .644 .203 .001 Age, Sex .051
Left Hand .501 .261 .029 Age, Handedness .127
Asymmetry .216 .206 .108 Handedness .094
NCCC
Overall Mean .672 .243 .002 None
Right Hand .770 .251 .008 None
Left Hand .359 .215 .031 None
Asymmetry .000 .000 .500 Handedness .047
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YNPRC = Yerkes National Primate Research Center, NCCC = National Center for Chimpanzee Care

Discussion

The results of this study are straightforward. First, intermanual performance differences on a tool use dipping task differed between left-, ambiguous- and right-handed chimpanzees. Further, these findings were reproducible between two samples of chimpanzees, suggesting the results are consistent. Second, heritability in average latency on the tool use dipping task was significant for each hand separately, as well as for the average between the two hands. Moreover, significant heritability in tool use performance was consistent between the two genetically isolated samples of chimpanzees. Third, asymmetries in tool use skill were not significantly heritable and this finding was also reproducible between the two chimpanzee populations. Finally, significant genetic and environmental factors influenced tool use performance for the left and right hands.

With respect to the findings on heritability, the results suggest there is a genetic basis for individual variation in motor skill, at least as measured by the latency scores on the tool use dipping task. The potential genetic contributions appear to be reproducible and therefore, less malleable in response to variation of non-genetic factors that might vary between different populations of apes. For example, the amount of experience with tool use and related enrichment devices between the NCCC and YNPRC chimpanzees are considerable, yet the heritability in performance is consistent between samples. We would further add that in the Hopkins et al. (2015) paper, heritability in tool use latency was also found to be significant in both the NCCC and YNPRC chimpanzees, though the methods for collection of the data differed from those used here. In short, performance data on tool use skill have been collected in two genetically isolated populations of chimpanzees using two slightly different methods and the results are consistent and reproducible. What potential genes may contribute to individual variation in tool use skill is unknown but warrants further investigation.

In contrast to heritability in overall mean latency, as well as average latency within the right and left hands, we did not find any consistent evidence of heritability of asymmetries in tool use performance, though the results for the overall sample approached conventional levels of statistical significance (p = .07). Recall from Table 1 that the PAQ scores were not significantly heritable for either the entire sample or within the NCCC or YNPRC populations. This suggests that genetic factors do not code for left-right differences in tool use performance, at least in chimpanzees and for this specific measure. Previous studies have found that chimpanzee hand preferences, including for tool use, and some measures of brain asymmetry are modestly heritable (Gomez-Robles, Hopkins, Schapiro, & Sherwood, in press; Hopkins, Adams, & Weiss, 2013; Hopkins, Misiura, Pope, & Latash, 2015) and the estimates of heritability from these previous studies were not all that different than the values for the entire sample reported in Table 1. Thus, the smaller sample size in this study may have weakened our ability to detect significant heritability in asymmetries for the tool use task.

It also should be noted that heritability for the right hand performance data was higher than the left for the overall sample and within both the NCCC and YNPRC populations. This could be interpreted as evidence for potential differential coding in left-right asymmetry in tool use skill. However, we would caution against interpreting these results without more direct evidence demonstrating that differences in heritability between the hands (or hemispheres) are associated with variation in gene sequences or asymmetries in gene expression (Blokland, vde Zubicaray, McMahon, & Wright, 2012; Strike et al., 2015). Indeed, we found significant genetic correlations in the latency scores for the left and right hands suggesting that common genes may potentially influence their performance. More generally, to what extent gene sequences or gene expression contribute to individual variation in asymmetries in hand skill or hand preference in humans, chimpanzees and other species remains entirely unclear from the extant data (Bisazza, Facchin, & Vallortigara, 2000; Bisazza, Sovrano, & Vallortigara, 2001; Sicotte, Woods, & Mazziotta, 1999; Signore, Chaoui, Nosten-Bertrand, Perez-Diaz, & Marchaland, 1991). For instance, in humans, estimates of heritability in hand preference and performance asymmetries are fairly small (D. Warren, M. , Stern, Duggirala, Dyer, & Almasy, 2012) and recent genome-wide association studies have not produced consistent results across studies (Armour, Davison, & McManus, 2014; Brandler et al., 2013; Brandler & Paracchini, 2014; Medland et al., 2005; Medland et al., 2009).

Unlike in Hopkins et al. (2015) and Sanz et al. (2016), in this study, we failed to find a complete dissociation between hand skill and hand preference. That is to say, mean latencies for the dominant compared to non-dominant hand were not significantly shorter across all handedness groups. For right-handed and ambiguously-handed chimpanzees, left-right differences in tool use performance were as would be predicted but, for left-handed chimpanzees, the mean latencies for the left and right hand were not significantly different. These findings are of interest for at least three reasons. First, there was no significant difference in the distribution of left-, ambiguously- and right-handed chimpanzees for tool use in this sample. Thus, the significant left-right differences among right-handed chimpanzees cannot be attributed to a significantly larger proportion of these individuals in the sample (i.e., increased statistical power). Second, though we cannot definitely rule it out, the lack of double dissociation between hand skill and hand preference is likely not attributable to differential learning or practice effects. That is to say, there is no reason to assume that left- and right-handed chimpanzees had unequal amounts of experience with their preferred compared to non-preferred hand. Thus, the group-level performance asymmetries observed in right-, but not left-handed, chimpanzees may be attributable to, as yet unknown, intrinsic factors. Third, the lack of difference in performance between the left and right hands within left-handed chimpanzees is not unique to the findings reported here on tool use. Hopkins (2018) reported data on performance asymmetries in grasping errors in a sample of 313 chimpanzees and showed that performance differences between the left and right hands were specific to right-handed apes. Thus, there is some consistency in the effect of hand preferences on left-right differences on performance measures in manual motor skill among chimpanzees.

We believe that the findings on the association between hand preference and performance asymmetries are also relevant to evolutionary models of hemispheric specialization. Notably, many evolutionary theories of hemispheric specialization emphasize the importance of selection for increased left hemisphere motor control in relation to human-specific adaptations such as posture, bipedalism, tool manufacture and use, and language (Bradshaw & Rogers, 1993; M. C. Corballis, 1992; M. C. Corballis, 2002; M. C. Corballis et al., 2012; Ocklenburg & Gunturkun, 2017). Further, most attempts to test these theories in nonhuman primates have focused on the assessment of hand preference with the implicit assumption being that preferred hand use reflects inherent differences in lateralization for motor control. The findings reported here do not entirely support this assumption and, indeed, only apply to right-handed chimpanzees. We would suggest that one reason performance asymmetries are specific to right-, but not left-handed, chimpanzees is because the preferred hand is compatible with the hemisphere that is dominant for motor control. In contrast, for left-handed chimpanzees, the effect of practice may potentially offset their inherent left hemisphere dominance for motor skill. Collectively, our findings suggest that some caution should be taken when assuming hand preferences reflect inherent specialization for motor control in the contralateral hemisphere.

Finally, the dissociation between performance asymmetries and hand preference in captive chimpanzees reported here is also germane to data from wild chimpanzees. A number of studies have reported hand preference data from wild and captive chimpanzees for different tool use actions (D. Biro et al., 2003; D Biro, Sousa, & Matsuzawa, 2006; Boesch, 1991; Boesch et al., 2017; Bogart et al., 2012; Harrison & Nystrom, 2008; Humle & Matsuzawa, 2009; Lonsdorf & Hopkins, 2005; Neufuss, Humle, Cremaschi, & Kivell, 2017; Sanz et al., 2016; Sugiyama, Fushimi, Sakura, & Matsuzawa, 1993). Though population-level biases are evident for some measures, such as termite fishing, ant dipping and wadge dipping, the direction of the bias varies between measures. With specific reference to termite fishing, when the cumulative data are summed across different field sites in wild chimpanzees, there are 79, 12 and 72 left-, ambiguous- and right-handed apes (see Table 2). Thus, there is no evidence of overall population-level bias in hand preference. However, there is an sex difference in the distribution of hand preference for termite fishing X2(2, N = 158) = 9.969, p = .007 (see Table 2). There were a higher proportion of right-handed males compared to females. For comparison, presented in Table 2 are also the hand preference data from 251 chimpanzees from the two captive populations studied in this paper and reported in Hopkins et al. (2015). In this combined sample, there were 91, 76 and 84 left-, ambiguous- and right-handed apes (see Table 2), and like the wild population, they do not exhibit a population-level bias. Further, there was no significant differences in the distribution of handedness between the NCCC and YNPRC colonies X2(1, N=251) = 0.804, p = .669 nor between the sexes X2(1, N= 251) = 3.627, p = .163. Thus, wild and captive chimpanzees appear to differ in two ways with respect to hand preference for termite fishing (wild) and simulated termite fishing (captive). First, wild chimpanzees exhibit a significant sex difference and captive apes do not. Second, as can be seen in Table 2, captive chimpanzees are also less lateralized than wild apes. That is to say, the percentage of ambiguously-handed is much lower in the wild (7% of the overall sample) compared to captive (30% of the overall sample) populations.

Table 2.

Summary of Handedness Data for Tool Use in Natural and Simulated Termite Fishing in Wild and Captive Chimpanzees

#L #R #A
Termite Fishing (Total) 79 72 12
 Field Site
 Gombe1 11 7 3
 Gombe2 12 4 1
 Fongoli3 17 13 4
 Goualongo4 39 48 4
 Males 29 41 8
 Females 48 30 2
Simulated Termite Fishing (Total) 91 84 76
 Captive Colony
 NCCC5 56 57 48
 YNPRC5 35 27 28
 Males 53 58 42
 Females 38 26 34
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Regarding performance asymmetries for termite fishing in wild chimpanzees, in the only published report, Sanz et al. (2016) recently found that the average latencies in termite fishing probes were significantly faster in the dominant compared to non-dominant hands in right- and left-handed chimpanzees. As with the Hopkins et al. (2009) and Sanz et al. (2016) report, there were unequal numbers of left and right hand responses within the left- and right-handed chimpanzees. Thus, what pattern in performance asymmetries would be found in circumstances in which an equal number of responses were obtained from each hand is unknown among wild chimpanzees. Notwithstanding, in the Sanz et al. (2016) report, when combining the average latency in termite fishing across all responses (e.g., for both the left and right hands), chimpanzees with a right-hand preference had significantly shorter latencies than left-handed apes, suggesting a left hemisphere dominance in manual motor control for this form of termite fishing. Recall that we did not find a main effect of hand preference on overall mean latencies in hand preference in this study. Thus, based on the findings reported here and those of Sanz et al. (2016), any effort to obtain additional performance measures of asymmetry for tool use actions in wild chimpanzees, and indeed all nonhuman primates, may be a fruitful area of future investigation and will shed important light on the evolution manual asymmetries

Acknowledgement

This research was supported in part by NIH grants NS-42867, NS-73134, HD-60563, and NSF INSPIRE grant 1542848 and Human Frontiers Science Program grant RGP0044 to WDH. The NCCC chimpanzees are supported by Cooperative Agreement U42–0D011197. The Yerkes Center and NCCC are fully accredited by the AAALAC International. American Psychological Association guidelines for the ethical treatment of animals were adhered to during all aspects of this study.

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