The evolution of human reproduction: A primatological perspective

Abstract

Successful reconstruction of any aspect of human evolution ideally requires broad-based comparisons with other primates, as recognition of general principles provides a more reliable foundation for inference. Indeed, in many cases it is necessary to conduct comparisons with other placental mammals to test interpretations. This review considers comparative evidence with respect to the following topics relating to human reproduction: (1) size of the testes, sperm, and baculum; (2) ovarian processes and mating cyclicity; (3) placentation and embryonic membranes; (4) gestation period and neonatal condition; (5) brain development in relation to reproduction; and (6) suckling and age at weaning. Relative testis size, the size of the sperm midpiece, and perhaps the absence of a baculum indicate that humans are adapted for a mating system in which sperm competition was not a major factor. Because sizes of mammalian gametes do not increase with body size, they are increasingly dwarfed by the size of the female reproductive tract as body size increases. The implications of this have yet to be explored. Primates have long ovarian cycles and humans show an average pattern. Menstruation is completely lacking in strepsirrhine primates, possibly weakly present in tarsiers and variably expressed in simians. The only other mammals reliably reported to show menstruation are bats. Three hypotheses have been proposed to explain the evolution of menstruation (eliminating sperm-borne pathogens; reducing the metabolic cost of a prepared uterine lining; occurrence as a side-effect of physiological changes), but no consensus has emerged. Copulation at times other than the periovulatory period is not unique to humans, and its occurrence during pregnancy is widespread among mammals. Although the human condition is extreme, extended copulation during the ovarian cycle is the norm among simian primates, in stark contrast to prosimians, in which mating is typically restricted to a few days when the female is in oestrus. The model of regular mid-cycle ovulation in simians is questionable. Gestation periods calculated on that basis show greater variability than in other mammals, and evidence from laboratory breeding colonies indicates that an extended mating period is matched by an extended period in which conception can occur. New evidence indicates that the noninvasive placentation found in strepsirrhine primates is not primitive after all. Furthermore, comparative studies reveal that such noninvasive placentation is not "inefficient". Evolution of highly invasive placentation in haplorhine primates is probably linked instead to immunological factors. Primates have relatively long gestation periods, and humans are average in this respect. However, there is evidence that humans show greater maternal investment during pregnancy in comparison with apes. Although the human neonate matches the typical precocial pattern of primates in most respects, a fetal pattern of brain growth continues for a year after birth, such that the human infant is "secondarily altricial" in terms of its dependence on parental care. Nevertheless, the "natural" lactation period of humans is probably about 3 years, fitting the expectation in comparison to other hominoids.

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