The integrative biology of reproductive functioning in nonhuman primates

As many as 70 years ago, researchers were looking to the study of NHPs to gain insights into reproductive function. These first studies were general studies of anatomy and physiology [ Matthews, 1946 ; Young & Yerkes, 1943 ] and mating/breeding behaviors in captivity [ Souri and Swani, 1962 ; van Wagenen, 1944/1945 ] in female monkeys and apes, and the 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 & Kumar, 1965 ], grivet monkey [ Butler, 1966 ], squirrel monkey [ Lang, 1967 ], baboon [ Hendrickx, 1967 ], lemur [ Evans & Goy, 1968 ], and gibbon [ Chaicumpa et al., 1969 ]. In this decade researchers began recognizing the importance of studying the content, collection, and storage, of semen in male monkeys [ Kraemer and Cruz, 1969 ; Mastroianni & Manson, 1963 ], though the emphasis was largely for the use of samples in artificial reproductive methods. More in-depth characterization of female NHP reproductive physiology was achieved in the 1970s, when studies of reproductive hormones under natural and experimental conditions were conducted in a variety of species at various stages of the reproductive 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 diagnosis in NHPs [ Gribnau, 1975 ; Hobson et al., 1975 ]. This period also saw the first studies into environmental influences (i.e., irradiated diet) on female reproductive functions [ Sialy et al., 1976 ]. In contrast, in this decade the preponderance of research into male NHP reproductive physiology remained primarily limited to evaluating semen collection methods [ Bush et al., 1975 ], though more detailed analysis of spermatozoa development and chemical composition 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 opposed 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, including 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 neural 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 development of fecal hormone analysis ( Risler et al., 1987 ). This breakthrough opened the door for future studies of wild primate reproductive endocrinology as well as energetic condition. At the same time, laboratory studies into male reproductive processes were being extended to examine endocrine effects on testicular 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, including dominance rank and pair-bond formation, on reproductive endocrinology and reproductive success being completed in both the field and laboratory [ Koenig, 1995 ; Silva & Sousa, 1997 ; Smith et al., 1997 ; Ziegler & Bercovitch, 1990 ]. Research in this decade also saw the emergence of a focus of research by Cameron and colleagues [ Cameron, 1997 ; Cameron et al., 1993 ; Williams et al., 1997 ], whose research focuses on the interaction between metabolic and psychological stressors on reproductive function in female macaques. Accordingly, we began to recognize NHPs as models for reproductive health issues of concern in humans such as stress-induced infertility 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 pollutants/toxins [ Foster et al., 1998 ], and social relationships [ Baker et al., 1999 ; Berard, 1999 ] on male reproductive function, though again this realm of research lagged behind what was known about female reproduction. The past 10–15 years have seen our understanding of the truly integrative nature of primate reproductive functioning strengthen, due in large part to contributions from the authors in this special issue. We now know the roles that the metabolic and psychosocial stressors [ Cameron, 2003 ; Williams et al., 2001a , b , 2007 ] play in female NHP fertility. We also know more about the role of neuropeptides and neurotransmitters in mediating the relationships 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 ; Fedigan & Jack, 2011 ; Goossens et al., 2006 ; Klinkova et al., 2005 ; Pope, 2000 ; Takahata et al., 2006 ]. This understanding has led to a natural progression toward the characterization of strategic interactions, for example, postcopulatory mechanisms, postcopulatory, and extragroup mating, and even sexual coercion by males, and their roles in reproductive success [ 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 heritability of fitness in macaques [ Blomquist, 2009 , 2010 ] while expanding our knowledge of female reproductive strategies to include behavioral and endocrine reproductive suppression [ Puffer et al., 2004 ; Saltzman et al., 2008 ] and selective investment in offspring [ Fite et al., 2005 ]. In this decade, we also learned more about male reproductive success with respect to paternal care and associated neurobiology, particularly in New World primates [ Fernandez-Duque et al., 2009 ; Nunes et al., 2001 ; Schradin et al., 2003 ; Ziegler et al., 2009a , b ], though not exclusively; see Buchan et al. [2003 ].

This special section is comprised of contributions from four of the five presenters in the 2011 symposium (T.E. Ziegler, J.A. French, M. Emery Thompson, and G.E. Blomquist). Like the symposium itself, 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 [2013 ] highlights research in her laboratory that has identified neural mechanisms underlying the social influences vis-à-vis olfactory cues on reproductive function and dysfunction in cotton-top tamarins ( Sanguinus oedipus ) and common marmosets ( Callithrix jacchus ). French [2013 ] adopts a “womb to tomb” perspective to describe years of work in his laboratory that has revealed the role of androgens in male marmosets’ ( Callithrix spp.) social phenotypes across the lifespan, which influence reproductive function and dysfunction. Emery Thompson [2013 ] summarizes research describing the reproductive ecology of wild female chimpanzees ( Pan troglodytes ), with particular foci on energetics and reproductive strategies. Finally, Blomquist [2013 ] presents an original study examining the roles of infant genetics and maternal variance in infant survivorship in free-ranging rhesus macaques ( Macaca mulatta ), using a novel quantitative genetics approach. Together, these contributions highlight not only the usefulness of the NHP as models for human reproductive processes, but also the truly integrative nature of the reproductive sciences. Further, these studies underscore the notion that primatology itself is increasingly becoming an integrative and multifaceted field of study. The studies presented here yield exciting avenues for multidisciplinary and collaborative research for future generations of primatologists.

The reproductive system represents a window into the integrative biology of primates. Multiple factors simultaneously influence reproductive functioning as well as dysfunction, including maternal variance, environmental factors, social relationships and interactions, genes, and hormones. Nonhuman primates (NHPs) serve as excellent models for the study of human reproductive processes owing to their high degree of genetic, physiological, morphological, and behavioral similarity. Though the majority of research into NHP reproductive function and dysfunction has occurred with female models, the articles in this special issue highlight this important model while emphasizing that the study of male NHP reproductive 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.