Abstract
BackgroundGerm lines are the cell lineages that give rise to the sperm and eggs in animals. The germ lines first arise from primordial germ cells (PGCs) during embryogenesis: these form from either a presumed derived mode of preformed germ plasm (inheritance) or from an ancestral mechanism of inductive cell-cell signalling (induction). Numerous genes involved in germ line specification and development have been identified and functionally studied. However, little is known about the molecular evolutionary dynamics of germ line genes in metazoan model systems.ResultsHere, we studied the molecular evolution of germ line genes within three metazoan model systems. These include the genus Drosophila (N=34 genes, inheritance), the fellow insect Apis (N=30, induction), and their more distant relative Caenorhabditis (N=23, inheritance). Using multiple species and established phylogenies in each genus, we report that germ line genes exhibited marked variation in the constraint on protein sequence divergence (dN/dS) and codon usage bias (CUB) within each genus. Importantly, we found that de novo lineage-specific inheritance (LSI) genes in Drosophila (osk, pgc) and in Caenorhabditis (pie-1, pgl-1), which are essential to germ plasm functions under the derived inheritance mode, displayed rapid protein sequence divergence relative to the other germ line genes within each respective genus. We show this may reflect the evolution of specialized germ plasm functions and/or low pleiotropy of LSI genes, features not shared with other germ line genes. In addition, we observed that the relative ranking of dN/dS and of CUB between genera were each more strongly correlated between Drosophila and Caenorhabditis, from different phyla, than between Drosophila and its insect relative Apis, suggesting taxonomic differences in how germ line genes have evolved.ConclusionsTaken together, the present results advance our understanding of the evolution of animal germ line genes within three well-known metazoan models. Further, the findings provide insights to the molecular evolution of germ line genes with respect to LSI status, pleiotropy, adaptive evolution as well as PGC-specification mode.
Highlights
Germ lines are the cell lineages that give rise to the sperm and eggs in animals
The genes for Drosophila were grouped into four categories as follows: 1) the lineage-specific inheritance (LSI) genes osk and pgc, which are directly involved in germ plasm function, and found only in certain insects, including Drosophila [2, 19]; 2) genes involved in regulating primordial germ cells (PGCs)-specification under the inheritance mode (“Inheritance”, N=13) in Drosophila studied to date; 3) orthologs to genes found to be involved in inductive signalling mode in mice or other models (“Induction”, N=15); and 4) genes involved in germ line formation regardless of mode (“Inh/Ind”, N=4) (Table 1)
In addition to studying these 34 germ line genes in Drosophila, we examined identifiable orthologs to this gene set in Caenorhabditis, as well as two Caenorhabditis LSI genes, and orthologs found in the fellow insect genus Apis (N=30 genes; four species studied; Additional file 1: Table S3), which likely exhibits induction
Summary
Germ lines are the cell lineages that give rise to the sperm and eggs in animals. The germ lines first arise from primordial germ cells (PGCs) during embryogenesis: these form from either a presumed derived mode of preformed germ plasm (inheritance) or from an ancestral mechanism of inductive cell-cell signalling (induction). Little is known about the molecular evolutionary dynamics of germ line genes in metazoan model systems. Germ lines are the specialized cell lineage contained in the gonads of sexually reproducing animals that give rise to the sperm and eggs. Much remains unknown about the molecular evolutionary dynamics of these germ line genes within metazoan model systems. The PGCs in some organisms arise from a presumed evolutionarily derived mode of maternally generated germ line determinants (inheritance), otherwise known as germ
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