Bacterial feeding nematodes in the order Rhabditida including Zeldia punctata (Cephalobidae) and Caenorhabditis elegans (Rhabditidae) differ profoundly in the buccal capsule parts and associated cells. We carried out a range of tests to determine which buccal capsule parts and cells are evolutionarily homologous between the representative species of the two families. Tests included reconstruction of the buccal capsule and procorpus with transmission electron microscopy (TEM), nuclei position and morphology using 4, 6-diamidino-2-phenylindole (DAPI) staining, and cell lineage using four dimensional (4D) microscopy. The lining of the buccal capsule of Z. punctata and additional Cephalobidae includes four sets of muscular radial cells, ma, mb, mc and md, in contrast to C. elegans and additional Rhabditidae, which has two sets of epithelial cells (e1, e3) and two sets of muscle cells (m1, m2). Cell lineage of a nematode closely related to Z. punctata, Cephalobus cubaensis, supports the hypothesis that in cephalobids the e1 and e3 cells become hypodermal cells or are programmed to die. Our findings contradict all previous hypotheses of buccal capsule homology, and suggest instead that ma and mb in Z. punctata are homologous to m1 and m2 in C. elegans respectively. We also hypothesize that ma and mb could be homologous to primary and secondary sets of stylet-protractor muscle cells in the plant parasitic Tylenchida.

Insight into the evolution of class Secernentea (Nematoda) for the purpose of providing a phylogenetic context for the model Caenorhabditis elegans is being gained from the use of molecular character sets. Such phylogenies provide a framework for mapping the evolution of diversity in some early-development characters for 70 species and 19 families of Secernentea. These characters include (i) whether AB and P1 blastomeres initially develop at the same (synchronous) or different (asynchronous) rates, (ii) whether AB and P1 are initially aligned along the linear axis of the embryo (tandem pattern) or obliquely (rhomboidal pattern), and (iii) whether the founder germ cell, P4, is established early, i.e., by the sixth cleavage, or later. Evolutionary polarity of characters was evaluated through outgroup comparisons. From our data the following inferences are made. The derived character, late establishment of P4, evolved primarily in the ancestor of the monophyletic groups Diplogastrina, Rhabditina, and Panagrolaimidae. Asynchronous development is convergent, defining one clade of Tylenchina as well as Cephalobina, and also arising independently in Aphelenchina. The rhomboidal embryo is ancestral to the tandem-pattern embryo that defines a second clade of Tylenchina. Early-embryo characters are congruent with the polyphyly of Cephalobina and Aphelenchina, as has been demonstrated by molecular phylogenies. Many aspects of early embryogenesis, rather than being highly conserved, evolve at a rate appropriate to defining taxa within Secernentea.

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