Nematode phylogeny and embryology

Abstract

Blaxter et al.¹ presented the phylogenetic tree of the phylum Nematoda based on the sequences of small subunit (SSU) ribosomal DNA (see also ref. 2). At the level of higher-order classification, this tree is substantially different to traditional taxonomic systems^3,4,5. The first branching of the SSU-based phylogenetic tree divides the nematodes into three big groups. Here we point out that three distinct patterns of early embryonic development reported for nematodes are in good agreement with this new classification. Differences in development could be more consistent with the natural nematode system than with the usual morphological criteria.

Main

The three nematode groups resulting from the first branching of the SSU-based phylogenetic tree are: clade I (orders Dorylaimida, Mononchida, Mermithida and Trichocephalida); clade II (orders Enoplida and Triplonchida); and a group subdivided into clades III-V that consists of Chromadoria and Secernentea.

Development of nematodes from clade II is different from development of nematodes of all other groups because the divisions in the early embryos (up to the eight-cell stage) are synchronous and produce blastomeres indistinguishable from each other by size, position and appearance⁵,⁶. Tracing cell fates with intracellular labels in group representatives Enoplus brevis⁶,⁷ and Pontonema vulgare (our unpublished results) shows that the blastomeres at these stages have no regular cell-lineage pattern. One of the two first-formed blastomeres may contribute to anterior or posterior, left or right, or intermediate parts of the embryo, and the endoderm precursor segregated at the eight-cell stage may derive from either blastomere.

In contrast, nematode embryos from clades III-V and I generate blastomeres that are already clearly distinguishable from each other after the first division. Embryonic development of nematodes from clades III-V has been well studied, and, in Caenorhabditis elegans, the complete stereotyped cell lineage has been followed⁸. In nematode embryos from this group, the anterior blastomere is named AB; its progeny divides in a synchronized pattern and gives rise to the particular structures of the animal. Predominantly posterior and internal parts of the embryo, including endoderm, derive from another blastomere of the two-cell stage — P₁(refs 5,⁸,⁹).

In nematodes from clade I, the first division also produces two blastomeres that are different to each other in size and fate, but are not homologous to AB and P₁ in nematodes of clades III-V. At the four-cell stage, two daughters of different blastomeres behave like AB progeny and another two resemble P₁ descendants. Endoderm in these species derives from the anterior blastomere of the first pair⁵,¹⁰,¹¹.

Thus, the cell-lineage patterns in the three large groups of nematodes seem to be very different. We realize that the above framework for different patterns of development in three taxonomic groups of nematodes is based on a few observations with varying degrees of reliability, but it gives straightforward, testable predictions.