Evolution of Predetermined Germ Cells in Vertebrate Embryos: Implications for Macroevolution

EVOLUTION & DEVELOPMENT 5:4, 414–431 (2003) Evolution of predetermined germ cells in vertebrate embryos: implications for macroevolution Andrew D. Johnson,a,b,* Matthew Drum,b Rosemary F. Bachvarova,c Thomas Masi,b Mary E. White,d and Brian I. Crotherd aDivision of Genetics, University of Nottingham, Queen’s Medical Centre, Nottingham NG7 2UH, UK bDepartment of Biological Science, Florida State University, Tallahassee, FL 32306, USA cDepartment of Cell and Developmental Biology, Weill Medical College of Cornell University, 1300 York Avenue, New York, NY 10021, USA dDepartment of Biological Science, Southeastern Louisiana University, Hammond, LA 70402, USA *Author for correspondence (e-mail: [email protected]) SUMMARY The germ line is established in animal embryos To determine which mechanism is ancestral to the tetrapod with the formation of primordial germ cells (PGCs), which give lineage and to understand the pattern of inheritance in higher rise to gametes. Therefore, the need to form PGCs can act as vertebrates, we used a phylogenetic approach to analyze a developmental constraint by inhibiting the evolution of basic morphological processes in both groups and correlated embryonic patterning mechanisms that compromise their these with mechanisms of germ cell determination. Our results development. Conversely, events that stabilize the PGCs indicate that regulative germ cell determination is a property of may liberate these constraints. Two modes of germ cell embryos retaining ancestral embryological processes, determination exist in animal embryos: (a) either PGCs are whereas predetermined germ cells are found in embryos predetermined by the inheritance of germ cell determinants with derived morphological traits. These correlations (germ plasm) or (b) PGCs are formed by inducing signals suggest that regulative germ cell formation is an important secreted by embryonic tissues (i.e., regulative determination). developmental constraint in vertebrate embryos, acting Surprisingly, among the major extant amphibian lineages, one before the highly conserved pharyngula stage. Moreover, mechanism is found in urodeles and the other in anurans. In our analysis suggests that germ plasm has evolved anuran amphibians PGCs are predetermined by germ plasm; independently in several lineages of vertebrate embryos. in urodele amphibians PGCs are formed by inducing signals. INTRODUCTION of an early developmental process, the germ cell deter- mining mechanisms among vertebrates, and its relation Variations in adult morphology arising during evolution are to developmental processes occurring before and after attributable to changes in developmental processes. The the pharyngula stage. Throughout we use the two major embryos of many vertebrates pass through a morphologically amphibian groups, the anurans (frogs and toads) and the similar stage, the pharyngula, occurring after the completion urodeles (salamanders and newts), as the prime examples for of neurulation, which is characterized by visible somites, discussion, but we also consider several issues at the level of prominent pharyngeal arches, and ventral flexure occurring the vertebrates. at the position of the neck (i.e., cervical flexure). Embryo- Anuran and urodele embryos begin to diverge before logical variation occurring after the pharyngula stage plays a gastrulation, at least a day before the pharyngula stage. When major role in diversification at higher order taxonomic levels compared within a phylogenetic context, we note that in all (Richardson 1999), and understanding the molecular me- cases early (prepharyngula) anuran development appears to chanisms underlying such diversification is currently an area be more derived and shows significant variability among of intense research. However, it is likely that variation of individual species, whereas urodele development retains earlier developmental processes, occurring before and ancestral features and is less variable within the various during the pharyngula stage, will result in the most pro- urodele lineages that have been examined. Because the germ found morphological variation, even though these events line develops by very different mechanisms in anuran and may also be the most highly constrained and resistant to urodele embryos, we next considered if this is related to the change (Raff 1996). In this review we consider the evolution observed differences in morphogenesis in these groups. 414 & BLACKWELL PUBLISHING, INC. Johnson et al. Evolution of germ cells in vertebrate embryos 415 In anuran embryos primordial germ cells (PGCs), the cells to the view that passage through the pharyngula stage that give rise to gametes, are of endodermal origin, and they represents a developmental bottleneck (for discussions of the are specified by the differential distribution of maternally ‘‘hourglass model’’ describing the pharyngula stage as a deposited germ cell determinants (known as germ plasm) to developmental bottleneck, see Elinson 1987; Raff 1996; the presumptive germ line blastomeres. Thus, from the Gerhart and Kirschner 1997). Changes in developmental inception of development, anuran PGCs are considered to processes occurring before the pharyngula stage, however, be predetermined by germ plasm. In urodele embryos PGCs may result in profound alterations to body structure, that is, derive from lateral plate mesoderm. Urodele embryos do not macroevolution (Raff 1996). An excellent example of early contain germ plasm, and so PGCs are specified later developmental changes correlating with differences in adult in development than in anurans. In urodeles PGCs form in morphology are found in the major amphibian lineages. response to extracellular inducing signals, not unlike those Pharyngula stage embryos and adults of Xenopus laevis (a that produce other mesodermal cell types. This is considered frog) and axolotl (Ambystoma mexicanum, a salamander) are regulative germ cell specification. When compared within a compared in Figure 1. Note that in Xenopus embryos (Fig. 1A) phylogenetic context, again the anuran mode of development the cervical region is reduced and does not undergo flexure appears to be derived, whereas the urodele mechanism (marking the future position of the neck) as it does in axolotls appears to be primitive to the tetrapods. Furthermore, when (Fig. 1B, arrow) or other vertebrates. X-rays of adult Xenopus considering the phylogeny of animals with and without germ and axolotl females show the vastly different skeletal structure plasm, the data suggest that germ plasm has evolved of these animals. The axolotl (Fig. 1, E and F) has a skeletal independently in several lineages of vertebrate embryos. structure similar to that of most vertebrates, including two Development of the notochord is a fundamental aspect of cervical vertebrae in the neck and 18 total vertebrae (arrow); vertebrate embryogenesis. We identified a strong correlation Xenopus (Fig. 1, C and D), in contrast, has a much shortened between the position of the notochord at the completion of vertebral column with only eight total vertebrae and one gastrulation and the mode of germ cell specification carried cervical vertebra. In addition, Xenopus also has the expanded out by embryos. Thus, regulative germ cell specification is pelvic girdle and lengthened hindlimbs typical of most frogs. correlated, in diverse groups, with the ancestral mode of Anurans and urodeles diverged from a common ancestor notochord development. In contrast, a derived process of about 250 million years ago (Cannatella and Hillis 1992; notochord development is observed in embryos that develop Milner 1992), and therefore it is likely that only one of the with a predetermined germ line. Within this context, we patterns of early development observed in the extant discuss how the emergence of germ plasm within an individual amphibians reflects the ancestral pattern. The other mode lineage may alleviate developmental constraints that are would be a derived pattern. The adult urodele body plan more imposed on morphogenetic movements by the process of closely approximates that of the common amphibian ancestor regulative germ cell specification and that regulative germ cell than does that of anurans (Duellman and Trueb 1986), specification may cause the retention of ancestral embryolog- particularly that of Xenopus, which is highly derived ical characters. In this way germ plasm may facilitate the (Cannatella and De Sa 1993). Here we compare various evolution of novel embryological features and thereby aspects of embryonic development. For clarification, the contribute to macroevolutionary divergence of adult form. anuran or urodele species referred to in each study are identified in text by superscripted letters that are listed in Table 1. We conclude that urodele embryos have retained EARLY MORPHOGENESIS DIVERGES BEFORE more features that can be considered primitive to vertebrates, THE PHARYNGULA STAGE IN AXOLOTLS and anuran embryos are generally more derived. Although AND XENOPUS comparative aspects of amphibian morphogenesis have been reviewed before (Hanken 1986; Malacinski et al. 1997), this Nothing in biology makes sense except when seen in the light of has not been addressed within a framework assuming a evolution. monophyletic origin of urodeles and anurans nor with T. Dobzhansky (1973) insights available from more recent work. The fact that vertebrate embryos from diverse taxa and very different early embryological forms (such as fish, amphibians, and mammals) converge on a similar morphology

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