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Association between hybrid status and reproductive success of captive male and female rhesus macaques (Macaca mulatta) at the California National Primate Research Center (CNPRC).

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American Journal of Primatology 73:671–678 (2011)
Association Between Hybrid Status and Reproductive Success of Captive Male
and Female Rhesus Macaques (Macaca mulatta) at the California National
Primate Research Center (CNPRC)
Department of Anthropology, California National Primate Research Center, University of California-Davis, Davis, California
California National Primate Research Center, University of California-Davis, Davis, California
Center for Biomolecular Science and Engineering, School of Engineering, University of California-Santa Cruz (UCSC),
Santa Cruz, California
The California National Primate Research Center (CNPRC) houses more than 1,000 rhesus macaques
(Macaca mulatta) of mixed Chinese–Indian ancestry. Most of these animals are kept in outdoor field
cages, the colony’s long term breeding resource. Since 2001, hybrids comprised between 4 and 49% of
the field cage populations, but in most cases have represented a maximum of 10% of those populations.
The increasing prevalence of hybrids is partly due to management efforts to distribute genetic diversity
effectively and minimize genetic subdivisions. However, other factors may also contribute to the spread
of hybrids within the colony, most notably variance in socio-sexual behaviors and physical attributes.
It is known that hybrids of some species exhibit heterosis, such as early maturation, that can enhance
reproductive success, and anecdotal observations of mixed groups of hybrid, Indian and Chinese
animals at the CNPRC suggest that hybrids are more sexually active. To determine whether hybrids
experienced a reproductive advantage, a study was conducted using birth records of 5,611 offspring
born in the CNPRC colony between 2003 and 2009. We found that while the degree of Chinese ancestry
(DCA) appeared to influence the maturational schedule of both males and females (maturation was
inversely related to proportion of Chinese ancestry), DCA had no independent effect on either male or
female RS or rank. Therefore, we have found no evidence that a hybrid phenotype confers an absolute
reproductive advantage in our colony. Am. J. Primatol. 73:671–678, 2011.
r 2011 Wiley-Liss, Inc.
Key words: hybridity; hierarchical rank; reproductive success; captive colony management
The ability to identify associations between
alleles and disease phenotypes can be diminished in
inbred or highly genetically homogeneous animals
because reduced genetic variation among research
subjects reduces the probability that rare causal
alleles will be present in the population. On the other
hand, the use of animals from different geographic
origins and/or their hybrids with very high genetic
variation can confound interpretations of phenotypic
differences of complex additive traits and disease
because it inflates the phenotypic variance of traits
with high heritability. Such variation requires the
use of a greater number of research subjects to detect
biologically meaningful differences between experimental and control groups. Therefore, a balance
must be struck between meeting the research
community’s need for genetically heterogeneous
stocks and a simple and less variable model system.
An advantage of using hybrid animals in
biomedical research is that hybrids with disease
r 2011 Wiley-Liss, Inc.
phenotypes whose frequency differs between the two
parental populations have an increased probability of
inheriting alleles linked to genes conferring susceptibility inherited from the parental population with
higher susceptibility. This is the underlying principle
of admixture mapping [Reich & Patterson, 2005],
which is useful for mapping disease-causing genetic
variants that vary in frequency between Indian and
Chinese rhesus macaques. The genomic location of
Contract grant sponsor: California National Primate Research
Center (CNPRC); Contract grant numbers: RR000169-48;
RR018144-07; Contract grant sponsor: NIH; Contract grant
numbers: RR005090; RR025871.
Correspondence to: Sree Kanthaswamy, Department of Anthropology, California National Primate Research Center, University
of California-Davis, Davis, CA 95616.
Received 15 November 2010; revised 23 February 2011; revision
accepted 25 February 2011
DOI 10.1002/ajp.20948
Published online 23 March 2011 in Wiley Online Library
672 / Kanthaswamy et al.
susceptibility genes with a higher frequency in
Chinese than in Indian rhesus macaques is marked
by an increase in the proportion of Chinese ancestry
at that location in a group of animals with a given
disease phenotype compared with a group of animals
without the disease.
At the CNPRC, pure Chinese rhesus macaques
are now maintained separately in one half-acre
outdoor field cage and several corncribs. Historically,
this was not the case. Since the early 1980s, imported
Chinese founders were hybridized with Indianderived animals [Roberts et al., 2000], and hybrids
now account for between 4 and 70% of the 1997
rhesus macaques currently maintained in the field
cages or North cages (NCs), each housing 80–180
animals [Kanthaswamy et al., 2010]. Since pure
Chinese rhesus macaques are no longer interbred
with hybrid or Indian rhesus macaques at the
CNPRC, the maintenance of animals with mixed
ancestry has triggered a predominantly one-way
gene flow of Chinese rhesus macaque alleles into
the Indian rhesus gene pool. The CNPRC colony
includes known hybrids of 1/8, 1/4, 3/8, 1/2, 3/4, 5/8
and 7/8 Chinese descent [Kanthaswamy et al., 2009].
Longitudinal data from 1970 to 2009 based on
demographic and pedigree information illustrate
that the number of hybrids have increased steadily
since the early 1980s as has the frequency of private
Chinese rhesus macaque short tandem repeat (STR)
alleles or STR alleles unique to the Chinese rhesus
macaques has increased (Fig. 1). The steep increase
in private Chinese STR alleles coincides with the
first introduction of Chinese founders into the colony
in the mind-1980s and underscores the rate at which
the genetic composition of the CNPRC rhesus colony
Fig. 1. Increase in Chinese and Indian private allele (alleles
unique to a population) frequencies over time at 14 STR loci.
This analysis is described in the Methods section.
Am. J. Primatol.
is changing (Fig. 2). According to import documentation and breeding records, only 640 pure Chinese
animals have been introduced into the colony.
This estimate is only a fraction of the approximated census count of 17,000 Indian-derived rhesus
macaques that have been reared at the colony since
its establishment. Therefore, the hybrids are predominantly responsible for the introgression of
Chinese alleles into the colony, especially since the
practice of crossing Indian animals with Chinese
imports has been discontinued.
The presence of hybrids with different degrees
of Chinese ancestry than F1 hybrids (Fig. 2) suggests
the absence of hybrid breakdown or dysgenesis
[Kanthaswamy et al., 2010]. In fact, hybridization
between Chinese and Indian rhesus macaques, two
regionally distinct and genetically disparate populations, has been demonstrated to result in novel highly
fit hybrid phenotypes, including longer male body
length, heavier male and female weight [Smith, 1986]
and an impulsive aggressive temperament [Champoux
et al., 1994, 1996, 1997]. These traits might influence
social rank and, consequently, reproductive success
(RS), because aggression is sometimes used for establishing and reinforcing social rank in rhesus macaques
and high levels of aggression are observed in breeding
groups during the breeding seasons when males and
females compete for mating partners [Bercovitch,
1997; Lindburg, 1971]. Rhesus females typically solicit
the sexual advances of males, often showing marked
preferences for some males over others [Southwick
et al., 1965], and the size of males is among many
factors that determine a female’s choice of a mate.
Body size, for example, is greater in rhesus than in
longtail macaques, and is an important determinant of
asymmetry of interspecies introgression from rhesus
to longtail macaques in Indochina [Evans et al., 2001;
Tosi et al., 2002] and might also be reflected in
intraspecies hybrid rhesus mating practices.
The heritability of body size and aggression has
been estimated in many animal breeds, including
Fig. 2. Increase in Chinese–Indian hybrids at the CNPRC over
time. This analysis is also described in the Methods section.
Hybrid Status and Reproductive Success / 673
rhesus macaques. An analysis by Clarke and O’Neil
[1999] showed that male Chinese-origin rhesus
macaques were heavier and longer than male Indian
rhesus but, as they reached adulthood, Indian adult
females grew much larger than Chinese adult
females. Therefore, a much greater sexual dimorphism exists between adult animals of Chinese
(or hybrid) ancestry than those of Indian ancestry.
If Fooden’s [1964] and Tosi et al.’s [2002] arguments
that introgression is strongly biased in the direction
of males of the larger rhesus macaques into females
of smaller longtail macaques can be applied to
captive rhesus macaques, then the choice of larger
mating partners by female rhesus macaques may
reflect female choice [Lindburg, 1971] and the larger
size of the Chinese and hybrid rhesus males might
enhance the RS of the smaller Indian females.
Current anecdotal reports of mixed groups of
hybrid and pure Indian rhesus macaques at the
CNPRC imply that hybrids encounter less aggression
than pure Indian animals, have priority of access to
estrous females and thus might sire more offspring
than pure Indian rhesus macaques. The increased
siring rate of hybrids is supported by Bernstein and
Gordon [1980] who report that the rates of agonistic
behavior in macaque hybrid groups are usually lower
than during initial group formation. In the CNPRC
scenario of mixed assemblages of Chinese and Indian
rhesus macaques, it is possible that social, morphological and behavioral attributes of the hybrids
contribute to their rise in the dominance hierarchy
(social rank) and increased their RS, causing the
asymmetric gene flow from the Chinese rhesus
genome into the Indian rhesus genome at the
CNPRC. Because of this, we postulate that sexual
selection, either female mating preference or higher
social rank of hybrids, has increased the RS of
hybrids in the colony and augmented their representation in the colony.
female with whom an individual animal secures
maternal attention/affection as an infant. STR
genotyping and parentage determination were conducted at the Veterinary Genetics Laboratory (VGL),
University of California, Davis, CA. Information on
STR markers, DNA extraction, PCR amplification of
STRs and fragment analysis of PCR products are
available elsewhere [Kanthaswamy et al., 2010].
The 14-STR genotypic dataset used for generating Figure 1 was obtained from 7,211 rhesus
macaques born between 1970 and 2009. Private
allele frequencies were computed using the GENEPOP software program [version 3.4; Raymond &
Rousset, 1995]. Based on the allelic frequencies at
the 14 STR loci, the program STRUCTURE 2.1
[Falush et al., 2003] was used to probabilistically
estimate the ancestry of 7,211 rhesus macaques
representing the 21 field cages including the
Chinese, Indian and hybrid animals whose RS were
assessed for this study (Fig. 2). The STRUCTURE
analysis was run at sweeps of 103 iterations after a
burn-in period of 103 without a priori defined
ancestral populations. The analysis was conducted
under the assumption of admixture (where samples
represent a mixture of two or more ancestral groups)
and correlated allele frequencies. In this analysis,
when a genotype reflects hybridity, or the absence of
genetic substructure, it will be assigned to one of the
two subpopulations (Indian and Chinese) with probability Q, the proportion of an individual’s genome
that originated from the Kth population [Falush
et al., 2003; Pritchard et al., 2000]. Individuals were
analyzed using this Bayesian clustering method to
probabilistically assign them to a proportion of
Chinese and/or Indian ancestry depending on the
fraction of their genomes that originated from their
The objectives of the analysis were to assess the
relative effects of hybrid status on an individual’s
annual rate of reproduction at a given age (measured
in years). This approach allowed us to determine not
only the effects of hybrid status on lifetime RS, but
also any attendant differences in maturational and
reproductive trajectories. We measured hybrid status
in terms of the degree of an individual’s genome that
was Chinese in origin or degree of Chinese ancestry
(DCA), which yielded an explanatory variable ranging
from 0 (100% Indian) to 1 (100% Chinese).
In addition to age and hybrid status, we also
considered the effects of rank in an effort to identify
how differences in DCA may actually influence RS
through its effect on rank. Rank was based on the
frequency of unidirectional aggression/submission
behaviors within dyads and indicates an individual’s
rank at a given age. We only considered individuals
who could be unambiguously ranked based on
The research was conducted using protocols
approved by the appropriate Institutional Animal
Care Committee (IACUC) and the American Society
of Primatologists (ASP) Principles for the Ethical
Treatment of Non Human Primates.
Nuclear Genetic Analysis, Parentage Analyses
and Population Genetic Analysis
All demographic, behavioral, pedigree and
genetic data were provided by the CNPRC. Pedigree
data used in this study were verified by STR-based
parentage assessments and when the genetic information was not available, parentage was assumed
based on sexual activity and circumstantial evidence.
This evidence includes the presence of the purported
parents in the same cage during the time of conception of an individual animal and the identity of the
Statistical Analyses
Am. J. Primatol.
674 / Kanthaswamy et al.
monthly assessments during the 2003/2009 study
Analysis was based on 5,611 breeding events
occurring between 2003 and 2009, involving 303
adult males (84 pure Indian, 214 hybrid and 5 pure
Chinese males) and 1,199 adult females (326 pure
Indian, 857 hybrid and 15 pure Chinese females). We
modeled male and female RS separately, because
male RS exhibited sixty-fold more variance than
female RS. Male RS followed a Poisson distribution
and was modeled as such using a log transformation.
Because of the seasonality of breeding in rhesus
macaques, females had, at most, one infant per year.
Therefore, from a longitudinal perspective (i.e. RS/
unit of age) female RS was a binary response (0 5 no
infant; 1 5 infant) and modeled using logistic regression, which assumes that the response is sampled
from a binomial distribution and uses a logit link
Model Comparison
Our analytical approach was one of model
comparison, using Akaike’s information criteria
(AIC) [Akaike, 1974] without small sample correction. AIC provides a measure of a model’s ability to
account for variance in the response variable, with
smaller values indicating a better fit. In addition, we
calculated Akaike weights, wi, [Burnham & Anderson,
1998] to assess the probability that a given model
was the true best-fit. We present model output and
weights for only those models that collectively
accounted for 95% of the available Akaike weight
[Burnham & Anderson, 1998].
Variance Components
Our data were longitudinal—individuals were
sampled multiple times over the course of their lives.
As such, it was characterized by repeated measures
clustered within subjects. To accommodate this
clustering we adopted a hierarchical modeling approach, allowing intercepts and responses to age to
vary by individual [Gelman & Hill, 2007]. We compared
models accommodating only inter-individual variance in intercepts to those also including variance
in slopes across age. We present the variance
components of only the best-fit models here. The
components of all others are available on request.
All analyses were run using the freely available
R software [R Development Core Team, 2008], using
the ‘‘lme4’’ package [Bates et al., 2008] for the
hierarchical modeling and the ‘‘bbmle’’ package
[Bolker, 2010] for the model comparison.
Candidate Model Set
The most basic models we considered were those
including only the main linear effects, individually
and together, of the three explanatory variables
Am. J. Primatol.
(DCA, age and rank). In addition, we also included
models containing a squared term for both age and
DCA to accommodate possible non-linear effects,
which simple plots of the data suggested may be
present. In addition to the main-effects models, we
also included an interaction between DCA and age,
as well as interaction between their squared terms
when present, because an individual’s DCA might
influence its life-history.
Male RS
The annual rate of male reproduction ranged
from 0 to 29 offspring per year, with a mean of
2.33770.112. Model comparison (Table 1) revealed a
model containing the independent effects of male
rank, age and age squared to be the best-fit, with
over 90% of the available model weight. The high
weight of this model indicates that it can be
considered the best-fit with reasonable certainty.
The model predicts that male RS was a decreasing
and decelerating function of increasing rank (Table 2
and Fig. 3A). In addition, it also predicts that male
RS was a polynomial function of age (Table 2), with
males experiencing a peak in annual reproductive
output when around 11 years of age (Fig. 3B).
While the top-ranked model carried over 90% of
the available weight, the second-ranked carried
nearly 10% and so was worth considering. This
TABLE 1. Parameter Number (k), Log Likelihoods
(logLik), AIC Values and Akaike Weights (wi) for Top
Two Models of Male RS
1,072.498 2,159 0.927
1,072.185 2,164 0.063
Model included random intercepts for Male ID (s2 5 3.108) and random
slopes for Male ID across Age (s2 5 0.042).
Model included random intercepts for Male ID (s2 5 3.126) and random
slopes for Male ID across Age (s2 5 0.042).
TABLE 2. Untransformed Effect Size (7Standard
Error) of All Variables in First and Second-Ranked
Models of Male RS
First ranked
Second ranked
Hybrid Status and Reproductive Success / 675
Fig. 4. Relationship between male RS and age. All lines are
relationship predicted by the second-ranked model. The dotted
line is the shape of the relationship when DCA 5 0, the dashed
line is at the mean, DCA 5 0.421, and the solid line is at DCA 5 1.
of the effects of rank stem from an association with
DCA (Table 3).
Female RS
Fig. 3. (A) Relationship between male RS and rank, where 1
indicates an alpha male. The line is the shape of the relationship
as predicted by the best-fit model (Table 2). (B) Relationship
between male RS and age. The line is the shape of the
relationship as predicted by the best-fit model (Table 2).
model contained the same effects as the top-ranked
model, as well as the additional effect of an
interaction between DCA and age (Tables 1 and 2).
While the standard errors for the two interaction
terms caution against generalizing the effect, estimates from the model suggest that there was an
effect of DCA on the maturational trajectories of
males. Specifically, they suggest that an increase
in DCA was associated with a later, but higher
reproductive peak (Fig. 4). When transformed, the
estimate of the main effect of DCA revealed that
it had little or no independent effect on male RS
(e 2.358–0.355 5 0.066). The fact that the estimates
of the effect of rank from the 1st and 2nd ranked
models were essentially the same suggests that none
When modeling female RS, model comparison
revealed a model containing the main effects of age,
rank and DCA and an interaction between DCA and
age (Table 3). As with the modeling of male RS,
the high weight of this model suggests that it was
the most likely best-fit within the candidate set. The
model predicts that rank had a negative effect on the
probability that a female had an infant in any given
season (Table 4 and Fig. 5). In addition, the model
predicts that this probability was also a polynomial
function of age, with a reproductive peak occurring
around 11–12 years of age (Fig. 6). Estimates of the
interaction term in the model suggest that the
timing and height of this peak varied with DCA
(Table 4). Specifically, the model predicts that
increase in DCA was associated with a later, but
higher reproductive peak (Fig. 6). As with the
modeling of male RS, however, the standard errors
of interaction terms caution against over-generalizing the effect.
In addition to all the effects contained by the
first ranked model, the second ranked also contained
a squared term for DCA and an interaction between
the polynomial for age and DCA (Tables 3 and 4).
Parameter estimates for the polynomial of DCA
indicate that it had little bearing on female RS as a
main effect (Table 4). In addition, it can be seen that
standard errors for the estimates of the interaction
suggest that its effect could not be reliably estimated.
This, together with the model’s low weight, suggests
Am. J. Primatol.
676 / Kanthaswamy et al.
TABLE 3. Parameter Number (k), Log Likelihoods (logLik), AIC Values and Akaike Weights (wi) for the Top Two
Models of Female RS
Rank1Age1 Age21DCA1 DCA:Age1DCA:Age2
Model included random intercepts for Male ID (s2 5 0.511) and random slopes for Male ID across Age (s2 5 0.027).
Model included random intercepts for Male ID (s2 5 0.511) and random slopes for Male ID across Age (s2 5 0.027).
TABLE 4. Untransformed Effect Size (7Standard
Error) of All Variables in First and Second-Ranked
Models of Female RS
First ranked
Second ranked
Fig. 6. Relationship between female RS and age. The dotted line
is the shape of the relationship when DCA 5 0, the dashed line is
at the mean, DCA 5 0.421, and the solid line is at DCA 5 1.
Fig. 5. Relationship between female RS and rank where 1
denotes the alpha female. The line is the shape of the relationship as predicted by the best-fit model (Table 4).
that the second-ranked model offered little further
insight into the factors mediating female RS beyond
that described by the top-ranked model.
Free-ranging Indian rhesus females reach
menarche by age three and can continue reproducing
until about 20 years of age [Rawlins & Kessler,
Am. J. Primatol.
1986]. Although after pubescence at age three or
three and a half years wild rhesus males can become
procreative by age four, studies reveal that males
usually do not sire infants until after age eight, or
after reaching full adult size [Bercovitch et al., 2003;
Dixson & Nevison, 1997]. Rhesus macaques of both
sexes have been observed to reach sexual maturity
sooner in captivity [Catchpole & van Wagenen, 1975]
and Smith [1993] speculated that the availability of
abundant food enables subadult males to achieve
adult size sooner, elevate in rank more rapidly and
more successfully compete with older males for
access to females in captivity than in the wild.
Hybrid status (DCA) was not observed to have
any direct effect on either male or female RS.
Interestingly, however, both male and female
maturation schedules were inversely related to
DCA revealed by their STR genotypes. An increase
in DCA was linked with a later, but higher
reproductive peak in both males and females,
although the timing and height of this peak varied
more conspicuously in females depending on their
DCA. Indian rhesus macaques matured earlier than
Chinese rhesus macaques, but the Chinese animals
exhibited much higher reproductive peaks than
Hybrid Status and Reproductive Success / 677
Indian animals after reaching maturity. The maturational schedules and reproductive peaks of male and
female hybrids lay between the schedules and
peaks of the two pure-bred forms. Smith and Scott
[1989] suggested that crossbreeding between rhesus
macaques of geographically diverse origins fosters
heterotic characteristics of significantly greater body
length and weight in Chinese–Indian rhesus macaque hybrids. This study, however, shows that hybrids
of both sexes represent intermediate fitness characteristics to either parental phenotypes in terms of
maturation and reproductive peaks, which is more in
line with the hybrid intermediacy hypothesis. The
differences between the Chinese and Indian rhesus
macaques could be attributed to how they were
derived. The Indian rhesus macaques come from
field cages that have been provisioned over several
generations, while the Chinese animals are firstgeneration descendants of recently imported founders. Therefore, the Chinese animals, especially the
females, exhibit adaptations to their cooler and drier
country of origin [Clarke & O’Neil, 1999] including
later maturation similar to temperate species as
observed here.
The relatively weak relationship between rank
and RS among males suggests that dominant males
were able to monopolize reproductive access to
estrous females to only a limited degree. According
to the priority of access (POA) model, in the
seasonally breeding rhesus macaque where multiple
females go into estrous simultaneously, high ranking
males enjoy diminished RS because they cannot
effectively restrict low ranking opponents from
impregnating sexually receptive females. Because
seasonal breeding fosters female choice, female
rhesus macaques do not always have to choose to
reproduce with top ranking males [Shively & Smith,
1985]. In a group of free-ranging rhesus macaques
during one breeding season, Berard et al. [1993,
1994] observed that the highest-ranking males
produced proportionally more offspring than their
subordinates, and yet they were cuckolded by low
ranking and extragroup males who had resorted to
‘‘furtive’’ mating tactics. Under the current housing
scheme at the CNPRC, the field cages accommodate
multiple sexually mature males to more closely
balance the sex ratio (which increases effective
population size) and better maintain group stability
[Kanthaswamy et al., 2010] and seem to have made
mate guarding by the dominant males quite ineffective,
The inclusion of males that have achieved subadulthood in this study could have compounded the
negative correlation between male rank and RS
[Bercovitch, 1986], although Smith [1993] disputed
that estimates of rank-related reproductive skew
are biased due to the inclusion of subadult males.
The relationship between female rank and RS
we observed is concordant with well-provisioned
situations that preempt differential female RS
resulting from the social hierarchy. This scenario
also undermines the POA model with the availability
of large numbers of fertile females and many
subordinate and subadult males that are sexually
mature. Inferences drawn from this study of 21
captive multi-male breeding groups do not support
the hypothesis that DCA affords hybrid males and
females a reproductive advantage. The study does,
however, suggest that hybrids of all genotype classes
are actively participating in the colony’s reproductive output and are thus propagating hybrid phenotypes at the CNPRC. This is concordant with present
breeding strategies to promote genetic heterogeneity
in the CNPRC colony [Kanthaswamy et al., 2010].
The environment in a captive colony influences
rhesus macaque social structure and behavior and
mating patterns differently than in natural settings.
The distribution and inheritance of fitness enhancing
characteristics such as early maturation, bigger body
size and long reproductive span have important
implications for developing the rhesus macaque as a
research model under closed colony management at the
CNPRC. Kanthaswamy et al. [2009, 2010] described a
dynamically changing pattern of genetic diversity and
hybridity within the CNPRC colony. As the rate and
consequences of hybridization fluctuate with time,
understanding hybrid fitness manifested in maturation
and RS and its genetic basis is a crucial first step in
predicting its evolutionary outcome and effectiveness
of colony management of research stocks. Questions
regarding the genetic impact of mixed ancestry
breeding must be answered, if CNPRC researchers
plan to continue to maintain hybrid populations in field
cages and corncribs within the colony.
This study was supported by the California
National Primate Research Center (CNPRC) base
grant (No. RR000169-48) by an ARRA supplement
awarded to S. K. and Nick Lerche, CNPRC
(No. RR018144-07) and NIH grants RR005090 and
RR025871 to D. G. S. We are grateful to Jenny Short
and Leanne Gill of the CNPRC for helpful discussions
that facilitated this manuscript. We thank Mark
Grote (Anthropology, UC Davis) for his helpful advice
on the statistics. These animals were managed in
compliance with Institutional Animal Care and Use
Committee (IACUC) regulations or in accordance with
the National Institutes of Health guidelines or the
US Department of Agriculture regulations prescribing
the humane care and use of laboratory animals.
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