Genomic imprinting and the evolution of sex differences in mammalian reproductive strategies

Adv Genet. 2007;59:217-43. doi: 10.1016/S0065-2660(07)59008-5.

Abstract

Two major developments have occurred that have influenced the evolution of sexually dimorphic reproductive strategies of mammals. Viviparity and development of a placenta is one such development, especially in small-brained rodent lineages, where there has been a major impact of placental hormones on the maternal brain. In the Old World primate/hominoid lineages, the massive expansion of the brain through growth of the neocortex has radically changed how reproductive strategies are determined. Genomic imprinting has played a significant part in both of these developments. Most of the imprinted genes investigated to date are expressed in the placenta and a subset are expressed in both placenta and hypothalamus. Based on phenotypes derived from targeted mutagenesis, a hypothesis is developed for the coadaptive evolution of placenta and hypothalamus, particularly in the context of neurohormonal regulation of maternalism. In small-brained mammals, maternalism places a severe restriction on sexual activity, which in the case of a female rodent is little more than several hours in a lifetime compared with the several weeks given over to maternalism. The consequent sparsity of oestrous, sexually receptive females imposes a rigorous competitive reproductive strategy in males, with the onus being on the male's ability to find oestrous females. This has resulted in a marked sex difference in the chemosensory system, particularly the VNO accessory olfactory system, for the engagement of male sexual behavior in response to oestrous females. Genomic imprinting, together with neonatal androgens, has also played a role in the developing accessory olfactory system and its role in detecting oestrous females. With the evolutionary expansion of the neocortex seen in Old World primates and hominids, reproductive strategies are complex and embedded in the social structure and hierarchies which characterize primate societies. Reproductive strategies depend far more on intelligent behavioral determinants than they do on hormonal determinants. In females, sexual activity is not restricted to oestrous periods, indeed most of the sexual activity is not reproductive. Male Old World primates continue to mate for years after castration, but loss of dominance status leads to a loss of sexual interest within days. The genetic basis for the expansion of neocortical development is complex, but those parts of the brain which have expanded are undoubtedly under the influence of imprinted genes, as studies using parthenogenetic and androgenetic chimeras and allometric analysis of brains across comparative phylogenies have shown. Sex differences in behavior owe much to social structure, social learning, and the deployment of intelligent behavioral strategies. The epigenetic effects of social learning on brain development have become equally as important as the epigenetic effects of hormones on brain development and both contribute to sex differences in behavior in large-brained primates.

Publication types

  • Review

MeSH terms

  • Animals
  • Brain / embryology
  • Brain / metabolism
  • Cell Lineage
  • Endocrine System
  • Evolution, Molecular
  • Female
  • Genomic Imprinting*
  • Humans
  • Male
  • Mammals
  • Mice
  • Models, Biological
  • Placenta / metabolism
  • Sex Characteristics
  • Sexual Behavior*
  • Sexual Behavior, Animal*