Causes and evolutionary consequences of primordial germ-cell specification mode in metazoans

Abstract

In animals, primordial germ cells (PGCs) give rise to the germ lines, the cell lineages that produce sperm and eggs. PGCs form in embryogenesis, typically by one of two modes: a likely ancestral mode wherein germ cells are induced during embryogenesis by cell-cell signaling (induction) or a derived mechanism whereby germ cells are specified by using germ plasm-that is, maternally specified germ-line determinants (inheritance). The causes of the shift to germ plasm for PGC specification in some animal clades remain largely unknown, but its repeated convergent evolution raises the question of whether it may result from or confer an innate selective advantage. It has been hypothesized that the acquisition of germ plasm confers enhanced evolvability, resulting from the release of selective constraint on somatic gene networks in embryogenesis, thus leading to acceleration of an organism's protein-sequence evolution, particularly for genes expressed at early developmental stages, and resulting in high speciation rates in germ plasm-containing lineages (denoted herein as the "PGC-specification hypothesis"). Although that hypothesis, if supported, could have major implications for animal evolution, our recent large-scale coding-sequence analyses from vertebrates and invertebrates provided important examples of genera that do not support the hypothesis of liberated constraint under germ plasm. Here, we consider reasons why germ plasm might be neither a direct target of selection nor causally linked to accelerated animal evolution. We explore alternate scenarios that could explain the repeated evolution of germ plasm and propose potential consequences of the inheritance and induction modes to animal evolutionary biology.

Keywords: epigenesis; germ line; preformation; primordial germ cell; spandrel.

Fig. 1.

Phylogenetic distribution of PGC specification mechanisms across Metazoa. Shown is a simplified phylogeny of animals (as per ref. 114), indicating whether members of a given clade exhibit inductive PGC specification (blue) or inheritance-mediated PGC specification (yellow), or whether the clade contains some members reported to use inheritance and others reported to use induction (green). Letters in circles at nodes indicate Bilateria (B) and Metazoa (M).