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Author Copy Only AUTHOR COPY ONLY REPRODUCTIONREVIEW Evolution of the germ line–soma relationship in vertebrate embryos Andrew D Johnson, Emma Richardson, Rosemary F Bachvarova1 and Brian I Crother2 School of Biology, Institute of Genetics, Queen’s Medical Centre, University of Nottingham, Nottingham, NG7 2UH, UK, 1Department of Cell and Developmental Biology, Weill Medical College of Cornell University, New York, New York 10065, USA and 2Department of Biological Sciences, Southeastern Louisiana University, Hammond, Louisiana 70402, USA Correspondence should be addressed to A D Johnson; Email: [email protected] Abstract The germ line and soma together maintain genetic lineages from generation to generation: the germ line passes genetic information between generations; the soma is the vehicle for germ line transmission, and is shaped by natural selection. The germ line and somatic lineages arise simultaneously in early embryos, but how their development is related depends on how primordial germ cells (PGC) are specified. PGCs are specified by one of two means. Epigenesis describes the induction of PGCs from pluripotent cells by signals from surrounding somatic tissues. In contrast, PGCs in many species are specified cell-autonomously by maternally derived molecules, known as germ plasm, and this is called preformation. Germ plasm inhibits signaling to PGCs; thus, they are specified cell-autonomously. Germ plasm evolved independently in many animal lineages, suggesting convergent evolution, and therefore it would be expected to convey a selective advantage. But, what this is remains unknown. We propose that the selective advantage that drives the emergence of germ plasm in vertebrates is the disengagement of germ line specification from somatic influences. This liberates the evolution of gene regulatory networks (GRNs) that govern somatic development, and thereby enhances species evolvability, a well-recognized selective advantage. We cite recent evidence showing that frog embryos, which contain germ plasm, have modified GRNs that are not conserved in axolotls, which represent more basal amphibians and employ epigenesis. We also present the correlation of preformation with enhanced species radiations, and we discuss the mutually exclusive trajectories influenced by germ plasm or pluripotency, which shaped chordate evolution. Reproduction (2011) 141 291–300 Introduction requirement for germ cell production, because defects in germ cell development affect species’ survival across Primordial germ cells (PGCs) are the precursor cells to the generations. Nevertheless, changes in somatic develop- eggs and sperm that comprise the germ line. PGCs are ment that would compromise the germ line cannot be specified in the early stages of metazoan development, tolerated, and so are not maintained (Johnson et al. segregating the germ line from the somatic cell lineages, 2003b). This brings into focus the paradox of germ cell or soma, that will give rise to the organ systems of the specification, because the mechanisms governing adult. The germ line and the soma play distinct roles in PGC specification are not conserved like those control- metazoan evolution. The sole function of the germ line is ling specification of somatic tissue. Instead, two distinct to transmit genetic information between generations, mechanisms of germ cell specification are known, and thereby maintaining a genetic lineage. The biological these show a punctuated distribution throughout the role of the soma, on the other hand, is to act as the vehicle animal kingdom (Extavour & Akam 2003, Johnson et al. that mediates germ line transmission (see Dawkins 1976). 2003a, Crother et al.2007). On the one hand, Thus, reproductive fitness is determined by the evolution preformation describes a mechanism in which PGCs of somatic traits in response to selective pressures. are specified cell-autonomously by molecules inherited However, the forces driving somatic diversity are from the egg, known as germ plasm. On the other hand is countered by constraints that resist change. So, for epigenesis, in which extracellular signals trigger PGC example, the mechanisms governing the development specification from pluripotent precursors. Remarkably, at of organs that sustain vertebrate physiology are conserved several taxonomic levels, both epigenesis and preforma- across vast phylogenetic distances because their func- tion exist in different lineages, and consequently, PGC tions are indispensable to survival of the adult. A less specification is governed by entirely different means in obvious, but perhaps more interesting, constraint is the closely related species. How and why this should be the q 2011 Society for Reproduction and Fertility DOI: 10.1530/REP-10-0474 ISSN 1470–1626 (paper) 1741–7899 (online) Online version via www.reproduction-online.org AUTHOR COPY ONLY 292 A D Johnson and others case is not understood, but it is appropriate to assume that somatic development. Because germ plasm functions it reflects a response to natural selection. Therefore, the in early development, while the somatic germ layers distribution of epigenesis and preformation must result are being programmed, and it renders germ cell from the influence each mode of germ cell specification specification independent of interactions with the has on the development of the soma. somatic environment, the presence of germ plasm might Understanding how the two modes of germ cell indirectly affect somatic gene regulatory networks specification evolved requires an elucidation of their (GRNs), liberating them to evolve without jeopardizing natural history, and for this purpose, vertebrate develop- germ line development. ment is particularly instructive. Vertebrate embryology is, Below, we discuss the theory that the force driving the in general, highly conserved, and vertebrate evolutionary evolution of germ plasm is enhanced evolvability of the history is well established, so it is possible to draw soma (Johnson et al. 2003b, Crother et al. 2007). We unambiguous conclusions about the ancestry of embry- summarize recent studies on germ plasm, focusing on ological traits. Thus, mammalian embryos do not contain vertebrates. However, we pay special attention to germ plasm (Eddy 1975); germ plasm is found in birds amphibians. Amphibian embryos are uniquely well (Tsunekawa et al. 2000), but not in turtles (Bachvarova suited to addressing how the germ line–soma relationship et al. 2009b); among amphibians, anurans (frogs) employ evolved, because the two modes of PGC specification are germ plasm, but urodeles (salamanders) do not (Smith found in the two major lineages, and these are 1966, Johnson et al. 2001); teleost embryos contain germ represented by experimental models, axolotls and plasm (Olsen et al. 1997, Yoon et al. 1997), but those of Xenopus, urodeles and anurans respectively. However, actinopterygian fish probably do not (Bachvarova et al. the recognition that epigenesis is conserved provides an 2009a). Viewing this pattern at a glance, two opposing interesting corollary. It suggests that the mechanisms hypotheses are possible. Germ plasm might be con- governing pluripotency are also conserved. Consistent served, but selectively lost in individual lineages, with this, ground state pluripotency, a cellular state from mandating the repeated emergence of epigenesis. which progenitors of the germ line or somatic lineages Alternatively, epigenesis is conserved, in which case can be derived, is conserved in the early embryos of germ plasm must have evolved in several vertebrate urodele amphibians and mammals; frog embryos, in lineages, independently. A resolution to this problem contrast, do not contain cells with equivalent potential becomes clearer when considering both modes of (Dixon et al. 2010). We discuss the apparent conflict specification within a phylogenetic distribution of other between predetermination and pluripotency in embryological traits. For example, mammals, basal vertebrate evolution, and we identify the dynamic nature reptiles, urodeles, and actinopterygians retain basic of the germ line–soma relationship as a major regulatory features of primitive chordate embryology (Cooper & component of the forces that shaped its pattern of Virta 2007, Shook & Keller 2008), and in each of these species diversification. taxa, PGCs arise by induction in the posterior lateral mesoderm (Bachvarova et al. 2009a). In contrast, PGCs form in very different locations in bird, frog, and teleost Preformation embryos, and germ plasm is inherited in each of these Since Weismann (1898) proposed the Germ Plasm embryos in different ways (Johnson et al. 2003b). From Theory, it has, until recently, been widely assumed that comparisons such as these, it has been concluded that preformation is conserved in the animal kingdom. In epigenesis is conserved and germ plasm evolved large part, this view emerged from studies that showed repeatedly (Johnson et al. 2001, 2003a, Extavour & that maternally inherited germ plasm was essential for Akam 2003, Crother et al. 2007). However, if this is true, it PGC development in frogs and flies (Smith 1966, raises the intriguing question: why has germ plasm Illmensee & Mahowald 1974), and that the structure of evolved so many times? germ plasm in these organisms is extraordinarily similar Though it is not conserved, the germ plasm of (Mahowald & Hennen 1971). Indeed, germ plasm in vertebrates and invertebrates accomplishes the same vastly divergent phyla is produced in oocytes and con- task; it inhibits the transcriptional
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