Abstract
BackgroundNematodes can be subdivided into basal Enoplea (clades 1 and 2) and more derived Chromadorea (clades 3 to 12). Embryogenesis of Caenorhabditis elegans (clade 9) has been analyzed in most detail. Their establishment of polarity and asymmetric cleavage requires the differential localization of PAR proteins. Earlier studies on selected other nematodes revealed that embryonic development of nematodes is more diverse than the essentially invariant development of C. elegans and the classic study object Ascaris had suggested. To obtain a more detailed picture of variations and evolutionary trends we compared embryonic cell lineages and pattern formation in embryos of all 12 nematode clades.MethodsThe study was conducted using 4-D microscopy and 3-D modeling of developing embryos.ResultsWe found dramatic differences compared to C. elegans in Enoplea but also considerable variations among Chromadorea. We discovered 'Polarity Organizing Centers' (POCs) that orient cleavage spindles along the anterior-posterior axis in distinct cells over consecutive cell generations. The resulting lineally arranged blastomeres represent a starting point for the establishment of bilateral symmetry within individual lineages. We can discern six different early cleavage types and suggest that these variations are due to modifications in the activity of the POCs in conjunction with changes in the distribution of PAR proteins. In addition, our studies indicate that lineage complexity advanced considerably during evolution, that is we observe trends towards an increase of somatic founder cells, from monoclonal to polyclonal lineages and from a variable (position-dependent) to an invariable (lineage-dependent) way of cell fate specification. In contrast to the early phase of embryogenesis, the second half ('morphogenesis') appears similar in all studied nematodes. Comparison of early cleavage between the basal nematode Tobrilus stefanskii and the tardigrade Hypsibius dujardini revealed surprising similarities indicating that the presence of POCs is not restricted to nematode embryos.ConclusionsThe pattern of cleavage, spatial arrangement and differentiation of cells diverged dramatically during the history of the phylum Nematoda without corresponding changes in the phenotype. While in all studied representatives the same distinctive developmental steps need to be taken, cell behavior leading to these is not conserved.
Highlights
IntroductionNematodes can be subdivided into basal Enoplea (clades 1 and 2) and more derived Chromadorea (clades 3 to 12)
Nematodes can be subdivided into basal Enoplea and more derived Chromadorea
Embryogenesis of Prionchulus sp To narrow this gap between Tobrilus with three and Romanomermis with six lineages we studied a second representative of clade 2B, Prionchulus sp. (Mononchida, n = 4)
Summary
Nematodes can be subdivided into basal Enoplea (clades 1 and 2) and more derived Chromadorea (clades 3 to 12). Embryogenesis of Caenorhabditis elegans (clade 9) has been analyzed in most detail. In this work we common ancestor of nematodes while Chromadorea include phylogenetically more derived species [2,5,6]. Our current picture of embryonic development in nematodes is essentially shaped by the striking similarity between the classic model system Ascaris megalocephala (Clade 8; Figure 1a; [7,8]) and Caenorhabditis elegans (clade 9; [9]; http://www.wormbook.org). Work on C. elegans and its closer relatives has provided an initial insight into the recent evolution of embryonic and postembryonic development in clades 8 to 10 and discloses wide homologies in features, phenotypes and cell lineages [4,10,11,12,13,14,15,16,17,18,19]. Generalizations from developmental characters of model organisms have to be taken with caution, because these organisms are often highly derived [20]
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