Research on primates reveals the myriad ways in which animals can alter their behavior to accommodate environmental change. 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 developmental psychology. We applaud this effort to unite these fields; indeed, it is likely that many aspects of human emotional behavior are important targets for natural selection.
Extrapolation of findings across age groups or species, however, is rarely straightforward, and the argument articulated by Del Giudice would be strengthened by greater sensitivity to the inherent limitations and challenges of such an enterprise. We illustrate this point in two ways. First, we underscore the need for precision when drawing analogies between humans and other primates by discussing how adaptive physiological mechanisms in other taxa may not act correspondingly in our own species. Second, we advocate caution when attempting to map specific biological systems onto relatively unspecified behaviors or feeling states. Emotions, such as those that mediate relationships in adult humans, are often difficult to assign clearly into those that are (or were) adaptive and those that are (or were) not.
An example of our first point is highlighted by Del Giudice's suggestion that human females practice facultative reproductive suppression by developing a lack of interest in sexual relationships when the social support systems necessary to help with childrearing are absent. While it is probable that humans are cooperative breeders, reproductive suppression in the context of cooperative breeding in other primates is accompanied by specific physiological, behavioral, and neuroendocrine mechanisms that have no parallel in humans. The best-known data concerning this phenomenon come from the marmosets and tamarins of the New World, who appear to utilize reproductive suppression in the context of kin selection (Hamilton Reference Hamilton1964). Subordinate individuals in these species assist in the rearing of the offspring of a much smaller number of related dominants, who are typically the only ones who become pregnant (Carlson et al. Reference Carlson, Ziegler and Snowdon1997). This is caused by a pheromonal–behavioral mechanism that regulates the process whereby dominant females prevent subordinate females living in the same group from ovulating (Barrett et al. Reference Barrett, Abbott and George1990). In fact, prevention of ovulation is the most widely used definition of reproductive suppression, with clear physiological correlates. For example, the ovaries of dominant females are 50% greater in volume than those of subordinates and have many more antral follicles, whereas subordinates lack corpus lutea and do not release sufficient lutenizing hormone for ovulation to occur (Abbott et al. Reference Abbott, Saltzman, Schultz-Darken and Tannenbaum1998). When a subordinate female is removed from her natal social group, however, this constraint is released, which can lead to pregnancy as few as eight days later (Ziegler et al. Reference Ziegler, Savage, Scheffler and Snowdon1987). In other words, it is the very presence of related females who could provide rearing support that causes reproductive suppression, not their absence. This is opposite to the scenario envisioned by Del Giudice. Although the term “reproductive suppression” does have other applications in the biological sciences, it is misleading to use this term to refer to mating avoidance in healthy females who are otherwise capable of reproducing successfully. In this case, Del Giudice's argument suggests a parallel between primate physiology and human behavior that is incorrect: There is no evidence indicating that such a phenomenon occurs in human females.
Our second and related point is that it is difficult to map clear, well-defined physiological mechanisms onto general behavioral constructs in humans. Del Giudice demonstrates creativity and thoughtfulness in attempting to link neurophysiology and evolution to a construct such as “attachment.” As he defines “attachment,” however (and indeed, how most psychologists now use the term), it is unlikely to be tied to any clear biological circuitry. We agree that discontinuity between infant and adult attachment is likely even though some of the same neural and endocrine systems, such as oxytocin-mediated social bonding, are involved. The author makes this point as well, suggesting that adrenarche represents a hormonal disconnect of behaviors advantageous in infancy from those that may be advantageous in adulthood. What is lacking is a precise, neurologically plausible definition as to what attachment means in human adults, as well as reliable tools for measuring it.
In infancy, attachment is characterized by a cessation of exploration, initiation of proximity to the caregiver, or distress if the caregiver is unavailable. The same behaviors are apparent in other primate infants as well, suggesting that intra-species comparisons of attachment may be justified in this specific case. In chimpanzees, for example, the mature caregiver provides a secure base from which the infant can explore and seek comfort, and one can interpret changes in hypothalamic-pituitary-adrenal axis activity as an index of the caregiver's effectiveness in reducing infant stress (Miller et al. Reference Miller, Bard, Juno and Nadler1986). In human adults, however, attachment is construed broadly as a personality variable that is not amenable to intercross-species comparisons analyses. For example, adult attachment is often operationalized as the coherence of narrative responses to questionnaires or interviews. Such information is undoubtedly a rich source of data, but this type of data taps into cultural expectations, is difficult to relate to the behavioral and physiological phenomena observed in human and nonhuman infants, and is not directly related to the social behaviors observed in other species. For these reasons, it is difficult to reach firm conclusions about the evolutionary significance of attachment as it is construed in human adults.
We admire Del Giudice's thesis as a noteworthy effort toward a better understanding of the evolutionary underpinnings of modern human adult relationships. Empirical studies of human biobehavioral plasticity, and the adaptive advantages such plasticity may confer, require thoughtful integration across species and across the ontogenetic spectrum, with special attention paid to the role of species-typical and species-atypical contexts. When done appropriately, such research is likely to excavate the biobehavioral processes that promote social competencies and health.
