Robert D. Martín

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.

Estimation of divergence times is usually done using either the fossil record or sequence data from modern species. We provide an integrated analysis of palaeontological and molecular data to give estimates of primate divergence times that utilize both sources of information. The number of preserved primate species discovered in the fossil record, along with their geological age distribution, is combined with the number of extant primate species to provide initial estimates of the primate and anthropoid divergence times. This is done by using a stochastic forwards-modeling approach where speciation and fossil preservation and discovery are simulated forward in time. We use the posterior distribution from the fossil analysis as a prior distribution on node ages in a molecular analysis. Sequence data from two genomic regions (CFTR on human chromosome 7 and the CYP7A1 region on chromosome 8) from 15 primate species are used with the birth-death model implemented in mcmctree in PAML to infer the posterior distribution of the ages of 14 nodes in the primate tree. We find that these age estimates are older than previously reported dates for all but one of these nodes. To perform the inference, a new approximate Bayesian computation (ABC) algorithm is introduced, where the structure of the model can be exploited in an ABC-within-Gibbs algorithm to provide a more efficient analysis.