Evolution of the germ line–soma relationship in vertebrate embryos

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.

Linking a Biological Mechanism to Evolvability

“…One empirical system in which evolvability has been invoked to explain species richness asymmetry in sister clades and differential rates of speciation, has been primordial germ cell (PGC) determination mechanisms [21][22][23][24]. Primordial germ cells are the precursor cells that eventually form eggs and sperm in the developing embryo.…”

“…As a constraint release, it has been argued that this increases the opportunities for the development of evolutionary novelties, some of which become key innovations that enhance speciation rates. Thus, lineages characterized by the determinative mode have high evolvability and this mode explains the increased rates of evolution of clades with that mode [6,21,23,27]. However, the use of evolvability in this sense, while seeming to fit the meaning of the concept, appears to be simply an un-quantified, abstract, buzzword.…”

Germline development in amniotes: A paradigm shift in primordial germ cell specification

“…Comparative analyses between taxa lead to the current view that the ancestral mechanism of PGC formation is induction 2, 20, 21, 22, 23, with the use of maternal specification and development of germ plasm occurring in several independent events during evolution (convergent evolution). In vertebrate anamniotes, maternal specification is employed by the teleost zebrafish 24, the sturgeon 25 (which belongs to the Acipenseriforms, considered ‘primitive fish’), and amphibian anurans 26, 27.…”

Cultivation and Biological Characterization of Chicken Primordial Germ Cells

“…It is precursors of the male and female gametes and develops into sperm, or egg cells (Nieuwkoop and Sutasurya 1979), which carry genetic information through sexual reproduction to future generations (Johnson et al 2011, Naito et al 2015. It is a pluripotent stem cell resource that has been discovered after embryonic carcinoma cells (ECCs), teratocarcinoma stem cells (TSCs) and embryonic stem cells (ESCs) (Matin et al 2004, Nayernia et al 2004.…”