Comparative survey of early embryogenesis of Secernentea (Nematoda), with phylogenetic implications

Abstract

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.

Differences in embryonic pattern formation between Caenorhabditis elegans and its close parthenogenetic relative Diploscapter coronatus

“…As such an arrangement has also been described for a variety of other nematodes in the classical literature (for references, see Malakhov, 1994), it can be asked whether it represents a more original pattern or is a derived character. Using outgroup comparisons, Dolinski et al (2001) concluded that within Rhabditida (clades 7-12) the rhombic 4-cell pattern as found in C. elegans is ancestral to the tandem pattern, which thus must have evolved more than once independently in individual nematode branches. The latter view is supported by our observations of linearly ordered blastomeres in the phylogenetically very With the division of P 3 four different variants (B1-C2) are generated, which eventually merge into a single pattern (D).…”

“…In the 2-cell stage the first somatic founder cell AB divides with a transverse orientation of the cleavage spindle, generating two daughters of equal developmental potential (Priess and Thomson, 1987). In contrast, its sister, the germline cell P 1 undergoes a rotation of the nuclear/centrosome complex (Hyman and White, 1987;Hyman, 1989) leading to a longitudinal orientation of the the C. elegans scheme, i.e., variants exist during the initial phase of development (Skiba and Schierenberg, 1992;Malakhov, 1994;Dolinski et al, 2001;Schierenberg, 2001;Schierenberg, 2005;Schulze and Schierenberg, 2008). A classic example is chromatin diminution in Ascaris accompanying the above-mentioned somagermline separation (Boveri, 1899).…”

“…Instead of a diamond-shaped blastomere arrangement in the 4-celled embryo, some nematode species show a linear grouping along the anterior-posterior axis (Malakhov, 1994;Dolinski et al, 2001). Such an arrangement is also found in a few close relatives of C. elegans, e.g., Diploscapter coronatus (clade 9; Tahseen et al, 1991).…”

The early embryonic development of the satellite organism Pristionchus pacificus: differences and similarities with Caenorhabditis elegans

“…Dolinski et al (2001) studied the time of establishment of the germline cell P 4 (late vs early), the arrangement of blastomeres in the four-cell stage (linear, partial linear or oblique) and whether AB and P 1 initially develop at the same (synchronous) or different (asynchronous) rates. The results showed that all character states were the same as in C. elegans.…”

“…Here, we present the early embryonic development of P. pacificus using 4D microscopy to analyse the cell lineage until the 50-cell stage. The first divisions of early embryonic development have been described for a number of nematodes over the entire phylum (Malakhov, 1994;Goldstein et al, 1998;Voronov & Panchin, 1998;Dolinski et al, 2001;Schierenberg, 2005;Lahl et al, 2006), whilst analyses up to the 50-cell stage are mainly restricted to members of the orders Rhabditida and Plectida (Skiba & Schierenberg, 1992;Spieler & Schierenberg, 1995;Lahl et al, 2003;Hasegawa et al, 2004;Laugsch & Schierenberg, 2004). Complete cell lineages have only been described for C. elegans (Sulston et al, 1983), Pellioditis marina (Houthoofd et al, 2003), Rhabditophanes sp.…”