Refuting the hypothesis that the acquisition of germ plasm accelerates animal evolution

Abstract

Primordial germ cells (PGCs) give rise to the germ line in animals. PGCs are specified during embryogenesis either by an ancestral mechanism of cell–cell signalling (induction) or by a derived mechanism of maternally provided germ plasm (preformation). Recently, a hypothesis was set forth purporting that germ plasm liberates selective constraint and accelerates an organism's protein sequence evolution, especially for genes from early developmental stages, thereby leading to animal species radiations; empirical validation has been claimed in vertebrates. Here we present findings from global rates of protein evolution in vertebrates and invertebrates refuting this hypothesis. Contrary to assertions of the hypothesis, we find no effect of preformation on protein sequence evolution, the evolutionary rates of early-stage developmental genes, or on species diversification. We conclude that the hypothesis is mechanistically implausible, and our multi-faceted analysis shows no empirical support for any of its predictions.

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

“…Our recent comparative large-scale molecular evolutionary analysis using a different study approach and different datasets, and spanning both vertebrates and invertebrates, did not support the predictions of the PGC-specification hypothesis (25). The assessment was based on genome-wide dN/dS of phylogenetically independent species pairs from 12 genera with different PGCspecification modes [the invertebrate genera Drosophila, Nasonia, Schistosoma, Anopheles, and Pristionchus (inheritance) and Tribolium, Echinococcus, and Apis (induction); and the vertebrate genera Falco and Xenopus (inheritance), and Alligator and Pan (induction)].…”

“…The assessment was based on genome-wide dN/dS of phylogenetically independent species pairs from 12 genera with different PGCspecification modes [the invertebrate genera Drosophila, Nasonia, Schistosoma, Anopheles, and Pristionchus (inheritance) and Tribolium, Echinococcus, and Apis (induction); and the vertebrate genera Falco and Xenopus (inheritance), and Alligator and Pan (induction)]. The results of these analyses supported the null hypothesis that PGC-specification mode has no consistent effect on protein sequence evolution, including on the evolution of the sequences of early developmental genes (25). Thus, these recent findings suggest that, at a minimum, the PGC-specification hypothesis does not hold in some animal genera, and that there is a good possibility that germ plasm is not strongly, or potentially even marginally, linked to rapid protein sequence divergence.…”

“…Furthermore, similar to the PGC-specification hypothesis, this hypothesis contends that inheritance accelerates evolution (early PGC specification, classified as determinative), and thus is discordant with examples suggesting no such effect in some animal lineages (induction taxa, presumably classed as stochastic; ref. 25). Nonetheless, whether ultimately well supported or disproven by future studies, the hypothesis highlights that the timing of induction varies among taxa with this PGC-specification mode, and that the stage of inductive signaling might be biologically or evolutionarily meaningful.…”

“…Furthermore, species richness itself appears unconnected to PGC-specification mode in multiple invertebrate lineages (25). Collectively, such examples appear inconsistent with the PGC-specification hypothesis (25).…”

“…Various other jawed vertebrates, including both preformation taxa (birds and teleosts) and induction taxa (lizards and eutherian mammals), each exhibit accelerated (nontypical) diversification rates (29). Furthermore, species richness itself appears unconnected to PGC-specification mode in multiple invertebrate lineages (25). Collectively, such examples appear inconsistent with the PGC-specification hypothesis (25).…”