PMCCPMCCPMCC

Search tips
Search criteria 

Advanced

 
Logo of nihpaAbout Author manuscriptsSubmit a manuscriptHHS Public Access; Author Manuscript; Accepted for publication in peer reviewed journal;
 
Behav Brain Sci. Author manuscript; available in PMC 2010 July 13.
Published in final edited form as:
Behav Brain Sci. 2009 February; 32(1): 41–42.
PMCID: PMC2903225
NIHMSID: NIHMS124537

Attachment and neuroendocrine profiles in infant and adult primates

Abstract

Comparing adults and infants of our own species must be considered as carefully as comparisons between humans and other primates. While many of the same neuroendocrine systems are present in each, there are also important behavioral and adaptive distinctions which, if not precisely defined, may lead to erroneous conclusions about evolutionary history.

Primate research often focuses on the ways in which animals can accommodate changing environmental circumstances by altering their behavior, which can provide a platform upon which selection may act. Del Giudice’s argument that human sexual behavior may also be facultative represents a significant contribution to this larger literature with important implications for both human evolutionary biology and psychology.

While we are highly sympathetic to the effort to unite these two fields, there are however specific arguments in this paper which would be strengthened by greater sensitivity to the limitations of extrapolation from one age group, and even from one species, to another. We illustrate our point in two ways. First, we underscore the need for precision when drawing analogies between humans and other primates by showing how well-defined, adaptive physiological mechanisms in other taxa may not act correspondingly in humans, and illustrate how assuming that they do can lead to faulty conclusions about human evolutionary ecology. Our second and related point is that it is not yet clear how well nonhuman behavioral data can support arguments about human feeling states, as most emotional behaviors are complex enough to make them difficult to assign clearly into those which are (or were) adaptive and those which are (or were) not. This is particularly true in such distinctly human phenomena as the type and style of our individual adult relationships, which are not as quantitatively well-defined as attachment phenomena observed in human infants and in other species.

Del Giudice’s suggestion that human females may practice facultative reproductive suppression by developing a lack of interest in sexual relationships when social support systems are absent (p 23) is an example of our first point. While it is probable that humans are cooperative breeders, reproductive suppression in the context of cooperative breeding in other primates comes with extremely specific physiological, behavioral, and neuroendocrine mechanisms that simply have no parallel in humans. The best known data concerning this phenomenon come from the marmosets and tamarins of the New World. Subordinate individuals in these species assist in the rearing of the offspring of a much smaller number of dominants, who are typically the only ones who become pregnant (Carlson et al., 1997). This works via a specific pheromonal-behavioral mechanism whereby dominant females prevent subordinate females living in the same group from ovulating (Barrett et al., 1990). In other words, it is the very presence of other females who could provide rearing support that causes reproductive suppression, not their absence. Furthermore, removal of such a female from her natal social support group releases this constraint, which can lead to pregnancy as few as eight days later (Ziegler et al., 1987). Prevention of ovulation, in fact, is the definition of reproductive suppression in this context, with clear physiological correlates. The ovaries of dominant females are 50% greater in volume than that of subordinates and have many more antral follicles, while subordinates lack corpus lutea and do not release sufficient lutenizing hormone for ovulation to occur (Abbott, Saltzman, Schultz-Darken & Tannenbaum PL, 1998). No such system is apparent in human females, regardless of their social circumstances. While the term “reproductive suppression” does have other, equally precise applications in the biological sciences, it should not be used to refer to mating avoidance in healthy females otherwise capable of reproducing successfully.

Leaving both precise definitions and other primates aside, we are furthermore not aware of any evidence supporting the proposal that human females separated from potential helpers experience anovulatory cycles any more frequently than those that do. Nor are we aware of conclusive evidence that such females become pregnant or successfully give birth any less frequently. In fact, there is evidence to the contrary which suggests that girls and women who lack social support from their families or from males are more likely to engage in risky sexual behaviors than those with adequate social support, and are also more likely to become pregnant as a consequence (e.g., Evans et al., 2004). The general problem with this argument is therefore twofold: first, that the analogy between humans and other primates fail, and second that the underlying argument may not hold true for modern humans themselves, making assertions about their adaptive value in our ancestors questionable at least.

Our second point is that it is difficult to map clear, well-defined biobehavioral phenomena onto ambiguous psychological constructs. Del Giudice demonstrates creativity and thoughtfulness in attempting to explicate a complex construct such as “attachment.” As he defines it, however —and indeed, how most psychologists now use the term – it is unlikely to translate directly onto either the behavioral repertoire of nonhuman primates or be clearly tied to any clear set of biological circuitry in humans who have matured past infancy. The author makes this point as well, suggesting that adrenarche represents a hormonal disconnect from those behaviors advantageous in infancy to those which may be advantageous as adults. We agree that discontinuity between child and adult attachment is likely even though some of the same neural and endocrine systems (such as oxytocin-mediated social bonding) are involved. What is lacking is precision in exactly what “attachment” means in human adults, and reliable tools for measuring it.

Bowlby’s seminal theoretical work on attachment focused on the human infant’s responses to stress as characterized by a cessation of exploration, initiation of proximity and contact seeking to the caregiver, and distress if the caregiver is unavailable. Using this definition, cross-species examinations of similar processes is possible and potentially fruitful: for example, one can focus on the ways in which the mature organism provides a secure base from which the infant can explore and seek comfort, and then interpret changes in stress hormones as an index of the caregiver’s effectiveness in reducing infant stress. While these notions of security and exploration have been empirically tested in nonhuman primates such as chimpanzees (e.g., Miller, Bard, Juno & Nader, 1986), it is unclear to us whether the additional psychological constructs that derive from personality theory and psychoanalysis are appropriate for this kind of analysis. Beyond infancy, “attachment” is not an index of distress when a vulnerable infant is separated from a caregiver, but now a set of responses to questionnaires or interviews, wherein the coherence of narratives about close relationships must be interpreted through the lens of cultural expectations.

We nonetheless recognize that this work represents a noteworthy effort toward a better understanding of the evolutionary underpinnings of modern human adult relationships. Future studies of human biobehavioral plasticity and the adaptive advantages it may confer will requires thoughtful integration of empirical data from social relationships to proteins, in species -typical and atypical contexts, across species, and across the ontogenetic spectrum. When done appropriately, such research is likely to excavate processes that promote social competencies and health.

Contributor Information

Seth D. Pollak, Department of Psychology, University of Wisconsin-Madison, W J Brogden Psychology Building, 1202 W Johnson St, Madison, WI 53706, USA, (608) 265-8190, ude.csiw@kallops..

Leslie J. Seltzer, Department of Anthropology, University of Wisconsin-Madison, 1500 Highland Avenue, Madison, WI 53705, USA, (608) 262-5148, ude.csiw@reztlesl.

References

  • Abbott DH, Saltzman W, Schultz-Darken NJ, Tannenbaum PL. Adaptations to subordinate status in female marmoset monkeys. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology. 1998;119(3):261–274. [PubMed]
  • Barrett J, Abbott DH, George LM. Extension of reproductive suppression by pheromonal cues in subordinate female marmoset monkeys, Callithrix jacchus. J Reprod Fertil. 1990;90(2):411–418. [PubMed]
  • Carlson AA, Ziegler TE, Snowdon CT. Ovarian function of pygmy marmoset daughters (Cebuella pygmaea) in intact and motherless families. Am J Primatol. 1997;43(4):347–355. [PubMed]
  • Evans AE, Sanderson M, Griffin SF, Reininger B, Vincent ML, Parra-Medina D, Valois RF, Taylor D. An exploration of the relationship between youth assets and engagement in risky sexual behaviors. J Adolesc Health. 2004;35(5):424, 21–30. [PubMed]
  • Miller LC, Bard KA, Juno CJ, Nadler RD. Behavioral responsiveness of young chimpanzees (Pan troglodytes) to a novel environment. Folia Primatol (Basel) 1986;47(2–3):128–142. [PubMed]
  • Zahed SR, Prudom SL, Snowdon CT, Ziegler TE. Male parenting and response to infant stimuli in the common marmoset (Callithrix jacchus) Am J Primatol. 2008 Jan;70(1):84–92. 2008. [PubMed]
  • Ziegler TE, Savage A, Scheffler G, Snowdon CT. The endocrinology of puberty and reproductive functioning in female cotton-top tamarins (Saguinus oedipus) under varying social conditions. BiolReprod. 1987;37(3):618–627. [PubMed]