The Evolution of the Human Placenta

5. Sex and the Placenta

5 Sex and the Placenta The diversity of placental structure, along with certain findings from molecular biology research, attest to the intense selective pressures this organ has been subjected to within the many mammalian lineages. It is an organ that has experienced considerable adaptive evolution. The placenta also appears to have affected basic genetic mechanisms within mammals that serve to regulate and drive mammalian biology. For example, among animals the phenomenon of gene imprinting appears to be mainly a mammalian genetic mechanism to guide offspring development. The placenta is obviously intimately associated with sexual reproduction. Although the placenta is derived from embryonic tissue, it can be considered an adaptation for female reproduction. However, the paternal genes are also represented in the placenta. The placenta has been suggested as a major site for maternal-paternal-fetal conflict, in the evolutionary sense. Of course, it is also a site where cooperation among these distinct genomes toward complementary fitness goals occurs. In this chapter, we examine sex determination and its effect on genetic regulation mechanisms in the fertilized egg and eventually in the placenta. We end the chapter with a discussion that starts to consider the phenomenon of gene imprinting and how existing mechanisms of DNA repair, silencing, and regulation of expression have been adapted to enable gene expression determined by gene origin. This powerful genetic regulatory mechanism appears to exist predominantly, if not solely, in mammals and flowering plants, two highly divergent taxa sharing a reproductive mechanism that allows intimate contact between maternal and offspring genomes. Sex Determination How do individuals become male or female? Sex differentiation begins during embryonic development. There are key time periods when the developmental pathways can be perturbed from their genetically programmed trajectory by  The Evolution of the Human Placenta hormones that pass through the placenta. This can affect both sex phenotype and sexuality. In other words, early life events can affect both the initial gonadal and other organ structures and the later developmental patterns and environmental-developmental interactions that result in sexual behavior. Sex differentiation is not the same as sex determination. Sex differentiation is the suite of developmental processes that result in the development of the gonadal, brain, and other organ structures that create phenotypic sex and later sexuality . Sex determination is the process by which sex differentiation is guided onto either the male or female pathways (Sarre et al., ). Sex determination in vertebrates falls into two basic categories: genetic or environmental (e.g., temperature-dependent). Among genetic mechanisms, the existence of sex chromosomes is fairly widespread; however, there are sexdetermining genes that are not on a sex chromosome per se. In some taxa (e.g., fish, birds) there are even sex reversals in individuals, where a female will become male or vice versa. Although it is not yet known what the ancestral condition for sex determination in vertebrates was, educated guesses abound. Some researchers have emphasized that the two categories of sex determination (genetic and environmental ) really represent opposite poles of a continuum (Sarre et al., ). In some taxa (for example, reptiles) both mechanisms are important (e.g., Shine et al., ). There are even species in which both mechanisms operate, as described below for the Australian three-lined skink. Temperature-Dependent Sex Determination It has long been known that incubation temperature has a dramatic effect on the sex ratio of hatchlings of all extant crocodilians, many turtles, and some lizards. There is also a family of birds (megapodes) in which the sex ratio of hatchlings is known to be temperature dependent. These birds do not sit on their eggs; rather, they bury their eggs in mounds that they construct out of leaves, dirt, and sticks. For example, the Australian brush turkey builds large compost mound nests in which the females bury their eggs. The eggs are warmed by the heat of decomposition. The males tend the nest, checking the temperature by thrusting their beaks into the mounds and adding or removing material. At temperatures around ºC (the mean for mounds measured in the wild) equal numbers of male and female chicks hatch. At cooler temperatures , more males than females hatch, while at warmer temperatures there are more female chicks (Göth and Booth, ). Sex and the Placenta  Multiple possible mechanisms can work to achieve variation in sex ratio of offspring due to incubation temperature. For example, in addition to temperaturedependent sex determination, there could be differential mortality between females and males at...