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 inf...

The placenta: a multifaceted, transient organ

“…Although the great apes also share haemochorial placentation, trophoblast invasion is deepest in the human [87]. This is consistent with the theory that greater access to the maternal blood supply facilitates growth of our large fetal brain [88]. However, the deep invasion comes at a price, for it is associated with an increased risk of complications of pregnancy, such as pre-eclampsia [89].…”

Maternal investment, life histories, and the costs of brain growth in mammals

“…The developmental basis of the evolution of large brain size in humans has often been considered to be an exceptional prolongation of postnatal brain growth, creating enhanced opportunities for environmental input to the developing brain (31)(32)(33). However, Vinicius (34) showed that the ways in which human brain and body growth patterns depart from those of other primates are more complex than this, including at least three distinct mechanisms: (i) a moderate extension of postnatal brain growth, (ii) a derived developmental allometry, and (iii) a retardation of postnatal body growth.…”

Testicular volume is inversely correlated with nurturing-related brain activity in human fathers

“…Although seasonal fluctuations in testes size are well documented in species with breeding seasons, surprisingly little is known about the relative stability of testes size in humans (23) or about the environmental, social, or nutritional factors that may influence it, and thus, it remains unclear whether greater testes volume is a cause or a consequence of male life-history strategies. If testicular volume is causal, individual differences in testes may be governed by evolved genetic influences, or they may be shaped by environmental factors analogous to the role of father absence in the timing of female menarche (36).…”

“…23). For example, among primates, monogamy and single-male polygyny are associated with smaller testes size compared with multimale, multifemale breeding systems.…”