Evolution of developmental mechanisms in nematodes

Abstract

The recent findings that key developmental genes are conserved across animal phyla have led to descriptions of evolutionary change in development based on the recruitment of these few molecules. This approach, however, encounters problems in assigning homology across long evolutionary distances. By contrast, reproducibility of the cell lineage of free-living soil nematodes (order Rhabditida) and conservation of larval blast cells across nematode species permit evolutionary comparisons of developmental mechanisms among nematodes at the cellular level. Such comparative studies uncover an unexpected flexibility of developmental mechanisms: Large evolutionary differences have been described between invariant and noninvariant lineages, in the cellular mechanisms specifying a given cell (for instance, the gonadal anchor cell), in the subcellular events leading to asymmetric divisions (for instance, the first division of the egg), and in redundant networks of cell interactions (for instance, those specifying the centered pattern of vulva precursor fates). Interestingly, redundancy of developmental mechanisms favored by selective pressure allows in turn for evolution of these mechanisms. Such evolutionary changes in developmental mechanisms specifying cell fates can occur in the absence of obvious morphological change, which rather correlates with evolution of cell fates per se: death, division, migration, and differentiation (for instance, in the reduction of the posterior gonadal arm in monodelphic species or in change in vulva position).

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

“…Embryonic-and postembryonic-stage investigations clearly demonstrate that cell fate often depends on induction signals from particular adjacent cells, but the details of signaling processes may vary even among closely related taxa (Schierenberg et al 1997;Sommer 1997;Sternberg and Félix 1997;Schierenberg 1998, 1999;Félix 1999). For example, in Cephalobidae, including Acrobeloides nanus, the different order of cell division leads to a different spatial arrangement of cells that is incompatible with certain cell-to-cell interactions found in C. elegans Schierenberg 1992, 1996;Schierenberg et al 1997).…”

“…Taxon-specific patterns of embryogenesis, including altered timing and arrangement of blastomeres, is particularly significant in relation to cell fate, based on interactions with adjacent cells (induction), versus subcellular events leading to asymmetric divisions (autonomy), or redundant networks of interactions (Félix 1999). In Rhabditina and Diplogastrina even the first cleavage may be regulated as a result of a specialized inductive determination of polarity (i.e., P1 versus AB), based on the point of sperm entry into the egg, and this character and its alternative (maternal determination of egg polarity) have been considered useful in defining the phylogeny of Secernentea (Goldstein and Hird 1996;Goldstein et al 1998).…”

“…In conclusion, an overview of divergent patterns of early embryogenesis through a wide range of Secernentea provides a basis for inferring the evolution of this diversity, and can help to target where more intensive studies on specification mechanisms might be most informative for interpreting phylogeny (Félix 1999;Schierenberg 2000). With the exception of axis of cleavage, most of the readily observed diversity of early embryogenesis in Secernentea is related to changes in timing, or heterochrony, which has been further considered to be a parameter for evolutionary classification of nematodes (Skiba and Schierenberg 1992).…”

“…Nematodes are good models for exploring the evolution of morphology and development (Fitch 1997;Sternberg and Félix 1997;Dolinski et al 1998;Félix 1999Félix , 2000Sommer et al 1999;Félix et al 2000). A focus of these nematode model systems has been the class Secernentea, which includes Caenorhabditis elegans (Maupas) Dougherty.…”

“…These provide a framework for mapping the evolution of early-development characters in Secernentea, and determining, for example, which of these characters are conserved at a level that defines major taxa and which are highly convergent. A key feature that allows comparisons to be made among Secernentea is that cell lineages within the class are said to be largely invariant, and blast cells are conserved to the extent that cell homologies are readily recognizable across taxa (Félix 1999;Félix et al 2000). This invariance in these nematodes and a few other organisms provides a powerful tool for examining evolutionary processes (Freeman and Lundelius 1992;van den Biggelaar and Haszprunar 1996).…”