American Journal of Primatology 75:197–201 (2013)
The Integrative Biology of Reproductive Functioning in Nonhuman Primates
AMANDA M. DETTMER*
Department of Psychiatry, University of Pittsburgh, Pittsburgh, Pennsylvania
At the 34th annual meeting of the American Society of Primatologists in 2011, the society organized an
interdisciplinary symposium entitled, “Reproductive Function & Dysfunction in Nonhuman Primates.”
The articles in this special section, excluding this introduction, represent the findings presented by
four of the five speakers in that symposium. The data presented highlight the myriad factors that
contribute to primate reproductive function and dysfunction, including hormones, genes, maternal
variance, environmental factors, social relationships, and strategic interactions. Collectively, these ar-
ticles emphasize the integrative nature of primate reproductive function, and highlight the importance
of the nonhuman primate as a model for human reproductive function and dysfunction in humans.
Am. J. Primatol. 75:197–201, 2013.
C ?2012 Wiley Periodicals, Inc.
Key words: reproduction; dysfunction; integrative; primate
The reproductive system represents a window
into the integrative biology of primates. Multiple fac-
tors simultaneously influence reproductive function-
ing as well as dysfunction, including maternal vari-
ance, environmental factors, social relationships and
interactions, genes, and hormones. Nonhuman pri-
of human reproductive processes owing to their high
degree of genetic, physiological, morphological, and
behavioral similarity. Though the majority of re-
search into NHP reproductive function and dysfunc-
tion has occurred with female models, the articles
in this special issue highlight this important model
while emphasizing that the study of male NHP re-
productive functioning is just as critical. Studying
the multiple factors that contribute to reproductive
success and failure in both sexes will yield valuable
information regarding similar processes in humans.
HISTORY OF NONHUMAN PRIMATE
As many as 70 years ago, researchers were look-
ing to the study of NHPs to gain insights into re-
productive function. These first studies were general
studies of anatomy and physiology [Matthews, 1946;
Young & Yerkes, 1943] and mating/breeding behav-
iors in captivity [Souri and Swani, 1962; van Wage-
relation of these variables to reproductive success.
The 1960s saw characterizations of the menstrual
cycle in a variety of female NHP species including
the chimpanzee [Erikson, 1963], loris [Ramaswami
rel monkey [Lang, 1967], baboon [Hendrickx, 1967],
lemur [Evans & Goy, 1968], and gibbon [Chaicumpa
et al., 1969]. In this decade researchers began recog-
nizing the importance of studying the content, collec-
tion, and storage, of semen in male monkeys [Krae-
mer and Cruz, 1969; Mastroianni & Manson, 1963],
though the emphasis was largely for the use of sam-
ples in artificial reproductive methods.
More in-depth characterization of female NHP
reproductive physiology was achieved in the 1970s,
when studies of reproductive hormones under natu-
ral and experimental conditions were conducted in
a variety of species at various stages of the repro-
ductive cycle [Boorman et al., 1974; Chandra et al.,
1971; Erikson & Wada, 1970; Kanagawa et al., 1973;
Parkin & Hendrickx, 1975], which ultimately led to
the development of techniques for pregnancy diag-
nosis in NHPs [Gribnau, 1975; Hobson et al., 1975].
This period also saw the first studies into environ-
mental influences (i.e., irradiated diet) on female re-
productive functions [Sialy et al., 1976]. In contrast,
in this decade the preponderance of research into
an article referenced herein was withdrawn, and the corrected
article was published online 6 December 2012.
*Correspondence to: Amanda M. Dettmer, Department of Psy-
chiatry, University of Pittsburgh, 3811 O’Hara Street, Pitts-
burgh, PA 15213. E-mail: firstname.lastname@example.org
Received 7 May 2012; revised 31 May 2012; revision accepted 6
Published online 23 July 2012 in Wiley Online Library
C ?2012 Wiley Periodicals, Inc.
198 / Dettmer
male NHP reproductive physiology remained pri-
marily limited to evaluating semen collection meth-
of spermatozoa development and chemical composi-
tion were beginning [Amann et al., 1976; Arora et al.,
1975], as were some studies into male contraceptives
[Laumas et al., 1978; Purandare et al., 1979].
The focus of NHP reproductive research shifted
in the 1980s, when we began to see studies directed
at understanding reproductive dysfunction (as op-
posed to normal function) in females. These studies
occurred primarily in the laboratory and included
environmental [Mohanty & Das, 1982] and drug
[Jaszczak, 1983; Mello et al., 1983; Smith & Asch,
1984; Mottet et al., 1985] effects on dysfunction, in-
cluding a greater understanding of the mechanisms
of the placenta [Berglund et al., 1989; Fazleabas
et al., 1989; Pepe & Albrect, 1984; Ramsey, 1981]
and uterus [Ducsay et al., 1983; Harbert & Spisso,
1980; Potgieter et al., 1985] during pregnancy.
We were also beginning to understand the neu-
ral underpinnings of female reproductive function
[Ferin, 1983; Hodges, 1985; Pohl & Hotchkiss,
1983], though detailed findings in this area of
research were forthcoming. Importantly, during this
decade, field researchers began the first studies of
wild NHP reproductive hormones owing to the de-
velopment of fecal hormone analysis (Risler et al.,
1987). This breakthrough opened the door for future
studies of wild primate reproductive endocrinology
ratory studies into male reproductive processes were
being extended to examine endocrine effects on tes-
ticular function [Mann et al., 1987; Shandilya et al.,
1982], though this area still lagged behind research
done in females.
In the 1990s, a more integrative approach
to studying female reproductive functioning was
emerging, with studies of social influences, includ-
ing dominance rank and pair-bond formation, on
reproductive endocrinology and reproductive suc-
cess being completed in both the field and labo-
ratory [Koenig, 1995; Silva & Sousa, 1997; Smith
et al., 1997; Ziegler & Bercovitch, 1990]. Re-
search in this decade also saw the emergence
of a focus of research by Cameron and col-
leagues [Cameron, 1997; Cameron et al., 1993;
Williams et al., 1997], whose research focuses on
the interaction between metabolic and psycholog-
ical stressors on reproductive function in female
macaques. Accordingly, we began to recognize NHPs
as models for reproductive health issues of con-
cern in humans such as stress-induced infertil-
ity and endometriosis [Schenken, 1997]. In this
decade, studies in male macaques were focused
on seasonal reproductive cyclicity [Chik et al.,
1992; Matsubayashi et al., 1991; Medhamurthy
et al., 1994], as well as on the effects of diet [Mattern
et al., 1993; Suhana et al., 1999], environmental pol-
lutants/toxins [Foster et al., 1998], and social rela-
tionships [Baker et al., 1999; Berard, 1999] on male
reproductive function, though again this realm of
research lagged behind what was known about fe-
The past 10–15 years have seen our understand-
ing of the truly integrative nature of primate repro-
ductive functioning strengthen, due in large part
to contributions from the authors in this special
issue. We now know the roles that the metabolic
et al., 2001a,b, 2007] play in female NHP fertility.
We also know more about the role of neuropeptides
and neurotransmitters in mediating the relation-
ships between various stressors and reproductive
function [Bethea et al., 2005, 2008; Centeno et al.,
2007; Cunningham et al., 2004]. During this time,
due in large part studied conducted in the field,
we have also seen a greater understanding of the
effects of kinship, social relationships, and group
dynamics in reproductive success for both male
and female NHPs [Altmann & Alberts, 2003; Fedi-
gan & Jack, 2011; Goossens et al., 2006; Klinkova
et al., 2005; Pope, 2000; Takahata et al., 2006]. This
understanding has led to a natural progression to-
ward the characterization of strategic interactions,
for example, postcopulatory mechanisms, postcopu-
latory, and extragroup mating, and even sexual co-
ercion by males, and their roles in reproductive suc-
cess [Doran-Sheehy et al., 2009; Emery Thompson
et al., 2008; Engelhardt et al., 2006; Knott et al.,
2010; Muller et al., 2007]. In the past 10–15 years,
we have also begun to learn about the heritabil-
ity of fitness in macaques [Blomquist, 2009, 2010]
while expanding our knowledge of female reproduc-
tive strategies to include behavioral and endocrine
reproductive suppression [Puffer et al., 2004; Saltz-
man et al., 2008] and selective investment in off-
spring [Fite et al., 2005]. In this decade, we also
learned more about male reproductive success with
respect to paternal care and associated neurobiol-
Duque et al., 2009; Nunes et al., 2001; Schradin
et al., 2003; Ziegler et al., 2009a,b], though not ex-
clusively; see Buchan et al. .
OVERVIEW OF THE SPECIAL SECTION
This special section is comprised of contributions
from four of the five presenters in the 2011 sympo-
sium (T.E. Ziegler, J.A. French, M. Emery Thomp-
son, and G.E. Blomquist). Like the symposium it-
self, this special issue is heterogeneous in nature in
that it comprises work performed in both New and
Old World primates, in both males and females, and
in both field and laboratory settings. Ziegler 
highlights research in her laboratory that has iden-
tified neural mechanisms underlying the social in-
fluences vis-` a-vis olfactory cues on reproductive
Am. J. Primatol.
Integrative Biology of Reproduction / 199
function and dysfunction in cotton-top tamarins
(Callithrix jacchus). French  adopts a “womb
to tomb” perspective to describe years of work in
his laboratory that has revealed the role of andro-
gens in male marmosets’ (Callithrix spp.) social phe-
notypes across the lifespan, which influence repro-
ductive function and dysfunction. Emery Thompson
 summarizes research describing the repro-
ductive ecology of wild female chimpanzees (Pan
troglodytes), with particular foci on energetics and
reproductive strategies. Finally, Blomquist 
presents an original study examining the roles of
infant genetics and maternal variance in infant sur-
vivorship in free-ranging rhesus macaques (Macaca
mulatta), using a novel quantitative genetics ap-
Together, these contributions highlight not only
the usefulness of the NHP as models for human
reproductive processes, but also the truly integra-
tive nature of the reproductive sciences. Further,
these studies underscore the notion that primatol-
multifaceted field of study. The studies presented
here yield exciting avenues for multidisciplinary
and collaborative research for future generations of
NOTE ADDED IN PROOF
manuscript by JL Cameron has been withdrawn,
and all references to it herein have been removed.
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