Elsevier

Advances in Genetics

Volume 59, 2007, Pages 217-243
Advances in Genetics

Genomic Imprinting and the Evolution of Sex Differences in Mammalian Reproductive Strategies

https://doi.org/10.1016/S0065-2660(07)59008-5Get rights and content

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.

Introduction

There have been a number of important developments in the evolution of mammalian reproductive success, important among which has been viviparity and placentation, lactation, and extended parental care. Viviparity is not unique to mammals, but unlike that found in certain fish and reptiles, it goes beyond the simple protection of incubating yolky eggs and involves the evolutionary development of a unique mammalian tissue, trophectoderm (Rossant, 1995). The most advanced form of placentation is invasive haemochorial in which trophoblast cells invade the maternal blood supply of the uterine endometrium, disrupting endothelial cells and thereby achieving direct contact with maternal blood (Moffet and Loke, 2006). This type of placentation characterizes rodents and primates, which are the dominant land animals of today. What might placentation have to do with sexually dimorphic behaviors? The placenta is integral to lactation and maternal care because both events are dependent on priming by hormonal secretions of the placenta. Together with pregnancy, these evolutionary developments have preoccupied female behavioral time budgets, such that sexual behavior is a relatively rare event for most female mammals. Female rodents take weeks to reach puberty, spend only hours sexually receptive, weeks pregnant, and weeks lactating until the offspring are weaned. Hence, sexually receptive females are at a premium, while most adult males are permanently sexually active. A male has potential for siring more offspring than a female, providing he is successful at finding oestrous females and competing for them with other males. Thus, in the context of reproduction, males and females have developed strategies subserved by sexual dimorphisms in behavior which optimize the reproductive success of their own sex (Emlen and Oring, 1977).

The mechanisms for regulating these dimorphic strategies in female reproductive behavior are strongly dependent on the epigenetic effects of placental hormones on the brain, which in turn have required coadaptation between placental development and hypothalamic development. In this chapter, I will consider how the placenta influences female reproductive behavior and the importance of imprinted genes in this context. Since imprinted genes are autosomal and expressed according to parent‐of‐origin, any such genes that determine brain development in rodents might therefore be expected, in utero, to develop a brain that is similar in males and females. The bias of phenotype in this developing brain is likely to be female based since it is developing and evolving under the influence of the same imprinted genes that are developing the placenta which produces the hormones that in turn regulate the hypothalamus for maternalism. Masculine traits are likely to be determined postnatally as a consequence of the epigenetic effects of hormone secretions from the male gonad. Indeed, this appears to be the case since male rodents castrated at birth are demasculinized and have the potential for female patterns of sexual behavior, while female rodents given androgen early postnatally adopt potential for masculine behavior patterns (Baum, 1979). Moreover, exposure to postnatal androgen in males or females does not prevent the brain from expressing parental care, provided sufficient exposure to pups is given that brings about sensitization (Meyer and Rosenblatt, 1980). An important question therefore is what are male androgens modifying in the developing rodent brain that determines adult male sexual strategies in behavior. A second important question is in what way has brain evolution and the development of a large neocortex such as that seen in monkeys and humans impacted on these phylogenetically older reproductive strategies and sexually dimorphic behavior.

Section snippets

Placental Regulation of Maternal Endocrine Function and Behavior

The placenta, developed from the cell lineage of fetal trophectoderm, exerts considerable influence on maternal endocrine function. Progesterone is the steroid hormone that dominates pregnancy and is necessary to sustain pregnancy. High levels of progesterone during pregnancy are a function of the fetal placenta either directly (primates) or indirectly (rodents) by production of placental hormones that sustain the ovarian corpus luteum. Progesterone has a broad spectrum of effects by acting on

Genomic Imprinting: Coadaptive Evolution of Brain and Placenta

The placental trophoblast is an extraordinary tissue capable of producing a vast range of endocrine secretions, which enable the fetus to regulate its own destiny. Most of these placental hormones function by acting on maternal receptors, an interaction that has required genomic coadaptation between mother and fetus. Hence, the functioning of two genomes (maternal and fetal) as part of a single phenotype (pregnant mother) provides a template for coadaptive selection pressures to operate. Early

Genomic Imprinting, Hypothalamic Development, and Behavior

The dual action of imprinted genes on the placenta and hypothalamus has both genetically and epigenetically ensured that the female reproductive strategy is strongly biased toward maternalism. Sexual behavior is a rare event in the life of a female rodent and is epitomized by a reflexive lordosis reactive response to the male. Male sexual behavior is very different, being a frequent behavioral preoccupation that involves proactively finding oestrous females and competing aggressively for them

Sex Differences in the Rodent VNO Pathway

The rodent vomeronasal system exhibits sexual dimorphisms at multiple levels along its projection pathway. The MeA, BNST, and MPOA are all larger in the male than female, while subsequent projections to the hypothalamic nuclei, particularly those concerned with female endocrine regulation and maternal care, tend to be larger in the female (Segovia and Guillamon, 1996) (Fig. 8.5). Lesions in discrete parts of this projection pathway enhance components of female typical behavior, whereas in the

Brain Evolution and Behavior: A Role for Genomic Imprinting

In early shrewlike mammals and other small‐brained rodents, the brain's regulation of behavior could be viewed as making an integrative contribution to physiological homeostasis. Such small brains may be considered as interfacing between internal bodily needs and the outside world in which the animal survives, serving to provide information about the habitat and social environment. Feeding is stimulated by hunger, sexual behavior is determined by the internal secretion of gonadal hormones, and

Conclusions

This chapter focuses on a relatively new area of mammalian gene regulation, genomic imprinting, that undoubtedly deserves further investigation in the context of sex differences in brain development and reproductive behavior. It is clear that imprinted genes play a major role in placental and hypothalamic development, and it is plausible to hypothesize coadaptive evolution of these structures, particularly in the context of maternalism. Maternalism has been integral to the female's reproductive

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