Selective accumulation of germ-line associated gene products in early development of the sea star and distinct differences from germ-line development in the sea urchin.
Introduction Germ cell segregation is an important problem in developmental biology, as it addresses how the fundamental distinctions between germ cells and somatic cells are initiated and maintained throughout development. The timing and mechanism of this segregation are also important for our understanding of evolution, for these influence the selective pressures that act on germ cells prior to gametogenesis, and so have important consequences for the selection of heritable variation (Extavour and García-Bellido, 2001). Primordial germ cells of many different species share intrinsic qualities that differentiate them from somatic cells, often long before the somatic gonads are formed. However, there has been a history of disagreement as to how germ cells may be identified, and when in development the germ line is specified. In this review, we examine descriptive and experimental data on the timing and mode of origin of the germ cell lineage throughout the animal kingdom. There are at least two distinct modes of germ line segregation in animals, both of which are well documented from experimental studies in model systems. These modes are summarised in Box 1. In some species, germ cells can easily be identified very early in embryogenesis, when their differentiation as germ cells is assured by the localisation of maternally inherited determinants before, or immediately following, fertilisation (‘preformation’). In other species, germ cells are not observed until later in development, and arise as a result of inductive signals from surrounding tissues (‘epigenesis’). To avoid confusion, the terminology that we will use in this review for germ cells and their precursors follows the nomenclature of Nieuwkoop and Sutasurya (Nieuwkoop and Sutasurya, 1979). When germ cells become sexually differentiated and enter the first stages of gametogenesis, they are collectively termed gonia (oogonia and spermatogonia). Through the processes of oogenesis and spermatogenesis, gonia become oocytes and spermatocytes, maturing finally into ova and spermatozoa, respectively. Many organisms generate their gonia from cells capable of almost indefinite rounds of asymmetric, self-renewing mitotic divisions; these cells are called germ line stem cells. The first cells that will give rise exclusively to germ cells by clonal mitotic divisions are called primordial germ cells (PGCs). The precursors to the PGCs, which are often initially morphologically indistinguishable from the surrounding somatic cells, are called presumptive primordial germ cells (pPGCs). These divide mitotically to produce one PGC and one somatic cell. Several aspects of germ cell morphology and function are clearly similar across many phyla of animals (Box 2). In spite of this, the mechanisms that generate germ cells appear to be highly variable, involving either prelocalised determinants or inductive processes. Previous monographs on comparative germ cell specification are now over 20 years old (Bounoure, 1939; Nieuwkoop and Sutasurya, 1979; Nieuwkoop and Sutasurya, 1981; Wolff, 1964). This review examines over 150 years worth of data on modes of germ cell specification in 28 metazoan phyla, expanding previous studies with the addition of recent molecular and experimental data. In this article we have also mapped the data onto a modern phylogeny of the Metazoa, to address the question of the ancestral mode and evolution of germ cell specification mechanisms. We conclude, in agreement with earlier surveys, that epigenesis is a more frequent mode of germ cell specification than preformation. This finding, together with data on germ cell origin in basal metazoans, suggests that epigenesis may have been the ancestral mechanism of early metazoan germ cell segregation. Our conclusion challenges a widely held view in the field of developmental biology (e.g. Wolpert, 1998) that epigenetic germ cell determination is an exception, and that most animals use localised cytoplasmic determinants to specify the germ line. In the following sections, we review data on the earliest specification of germ cells in development, in both the Germ cells play a unique role in gamete production, heredity and evolution. Therefore, to understand the mechanisms that specify germ cells is a central challenge in developmental and evolutionary biology. Data from model organisms show that germ cells can be specified either by maternally inherited determinants (preformation) or by inductive signals (epigenesis). Here we review existing data on 28 metazoan phyla, which indicate that although preformation is seen in most model organisms, it is actually the less prevalent mode of germ cell specification, and that epigenetic germ cell specification may be ancestral to the Metazoa.