Regulative germ cell specification in axolotl embryos: a primitive trait conserved in the mammalian lineage

Abstract

How germ cells are specified in the embryos of animals has been a mystery for decades. Unlike most developmental processes, which are highly conserved, embryos specify germ cells in very different ways. Curiously, in mouse embryos germ cells are specified by extracellular signals; they are not autonomously specified by maternal germ cell determinants (germ plasm), as are the germ cells in most animal model systems. We have developed the axolotl (Ambystoma mexicanum), a salamander, as an experimental system, because classic experiments have shown that the germ cells in this species are induced by extracellular signals in the absence of germ plasm. Here, we provide evidence that the germ cells in axolotls arise from naive mesoderm in response to simple inducing agents. In addition, by analysing the sequences of axolotl germ-cell-specific genes, we provide evidence that mice and urodele amphibians share a common mechanism of germ cell development that is ancestral to tetrapods. Our results imply that germ plasm, as found in species such as frogs and teleosts, is the result of convergent evolution. We discuss the evolutionary implications of our findings.

Blimp1 and the Emergence of the Germ Line during Development in the Mouse

“…This is apparently a predominant mechanism in the Metazoa and it operates in mammals. 3,8 However, until recently, the molecular mechanisms underlying this manner of germ cell specification and the properties of the resultant founder population of primordial germ cells (PGCs) have been poorly defined.…”

Evolution of the germ line–soma relationship in vertebrate embryos

“…To resolve the problem that two distinct modes of germ cell specification exist in vertebrates, Johnson et al (2001Johnson et al ( , 2003a noted the parallels of development in axolotls and mice, and proposed that epigenesis, not predetermination, is conserved. Strong support for this hypothesis comes from studies with turtles, representing reptiles.…”

“…In contrast, PGCs form in very different locations in bird, frog, and teleost embryos, and germ plasm is inherited in each of these embryos in different ways (Johnson et al 2003b). From comparisons such as these, it has been concluded that epigenesis is conserved and germ plasm evolved repeatedly (Johnson et al 2001, 2003a, Extavour & Akam 2003, Crother et al 2007). However, if this is true, it raises the intriguing question: why has germ plasm evolved so many times?…”

“…This brings into focus the paradox of germ cell specification, because the mechanisms governing PGC specification are not conserved like those controlling specification of somatic tissue. Instead, two distinct mechanisms of germ cell specification are known, and these show a punctuated distribution throughout the animal kingdom (Extavour & Akam 2003, Johnson et al 2003a, Crother et al 2007). On the one hand, preformation describes a mechanism in which PGCs are specified cell-autonomously by molecules inherited from the egg, known as germ plasm.…”

Linking a Biological Mechanism to Evolvability

“…Previous work by Johnson et al [26]; Crother et al [6 , 21] has shown that groups that exhibit the determinative mode are significantly more species rich in general and are always more species rich than their sister clade with the induced mode. For example, urodeles are induced and anurans are determinative and anurans have an order of magnitude more species.…”