An Overview of Annelid Development
All annelids born by gametic reproduction, be it sexual or parthenogenetic, undergo similar phases of early cleavage, blastulation, and gastrulation. Further development is highly variable depending on lineage and life history strategy. The diversity of annelid life histories can be grouped in two initial categories: indirect and direct developers. Indirect developers hatch as some type of trochophore larva, which comprises the rudiments of the anterior and posterior terminal regions of the adult worm (Figure 4.IB). During post-embryonic development, this larva intercalates a variable number of segments between these rudiments, and then undergoes a meta- morphic process into a juvenile form, usually associated with a habitat shift. Post- metamorphic juveniles go on adding segments from a posterior subterminal region known as the segment addition zone (SAZ), which together with the developing new segments, form the posterior growth zone (PGZ). In direct developers, embryonic development eschews the larval stage, instead generating a juvenile with many segments at hatching time (Anderson 1973). Most annelids continue adding segments at their PGZ throughout their life, but a few lineages have evolved determinate growth and fixed segment numbers. In leeches, which have a fixed segment number, hatchlings are born with their full complement of segments and have no active post- embryonic PGZ (Anderson 1973).
Early Embryonic Development
Early embryonic development in annelids provides classic examples of spiralian development (Anderson 1973). The fertilized zygote has an intrinsic animal-vegetal axis along which the first and second cleavage planes are extended, and which corresponds roughly to the future anteroposterior axis. In contrast to mollusks (Freeman and Lundelius 1992), most annelids that have been studied exhibit unequal first and second cleavages (Dohle 1999). These unequal cleavages yield a four-cell stage with identifiable cells, which thus defines the second axis of the embryo, corresponding roughly to the future dorsoventral axis. By convention, these first four blasto- meres are designated as А, В, C, and D macromeres, with D giving rise primarily to dorsal progeny and В to ventral progeny in the early embryo; A and C contribute left- and right-lateral fates, respectively (Figure 4.2A, E). The next four cleavages are usually unequal and occur with obliquely equatorial planes of division, yielding successive quartets of smaller micromeres in animal territory that are offset in either a clockwise or anticlockwise manner from the parent macromeres (Figure 4.2B-C, F-G). Between consecutive rounds of division, the location of the spindles rotates 90 degrees in alternating clockwise and counterclockwise direction (as seen from either of the animal-vegetal poles). This series of (usually unequal) cleavages eventually results in a 64-cell embryo showing a pattern reminiscent of a spiral when seen from the anterior animal pole and is thus termed “spiral cleavage” (Figure 4.2D, H). Spiral cleavage is a landmark of spiralian development, is often highly stereotyped, and has been found to be quite conserved across many groups of protostome animals, including annelids, mollusks, nemerteans, and flatworms (Henry 2014).
Spiral cleavage is difficult to visualize and to describe, as attested both by early attempts to describe this developmental process during the 19th century, and by students past and present trying to understand it (Anderson 1973). At the close of the 19th century, E.B. Wilson (1892) and E.G. Conklin (1897) developed a nomenclature to name individual blastomeres at each step of cleavage, thus allowing for more precise descriptions and more meaningful comparisons across species. This system was developed initially for species showing unequal rounds of cleavage that left smaller blastomeres toward the anterior, animal pole of the embryo and larger blastomeres toward the posterior, vegetal pole, and thus the nomenclature suggests a stem cell-like nature of the posterior blastomeres. While investigation in further species revealed this not to be accurate, the naming system was already deeply embedded in most descriptive and comparative work and is still widely used.
As described earlier, the zygote initially undergoes two rounds of meridional cleavage resulting in an embryo whose four cells are designated А, В, C, and D. The third cleavage results in animal and vegetal quartets of cells. Each of the blastomeres
FIGURE 4.2 Early annelid development: cleavage and blastula fate maps. A-H: Comparison of early cleavage of a small oligolecithal egg of an indirect-developing polychaete and the large yolky egg of a direct developing clitellate. Green double arrows show daughter cells; degree of cleavage inequality is approximated by relative arrowhead size. Animal pole views except where otherwise indicated. A-D: Early cleavage of Oxydromus obscurus (Errantia: Hesionidae), a polychaete with small eggs (-60 pm) and little yolk. A: 4-cell embryo resulting from two rounds of equal cleavage. B: 8-cell embryo after an equal third cleavage. C: 16-cell embryo after a roughly equal fourth cleavage. D: 32-cell embryo, showing the trunk ectoderm precursor 2d1 (dark blue), trunk mesoderm precursor 4d (red), and endoderm precursors (purple); vegetal pole view. E-F: Early cleavage of Tubifex tubifex (Clitellata: Naididae), a clitellate with large, yolky eggs (-450 pm). E: 4-cell embryo resulting from two rounds of unequal cleavage. F: 8-cell embryo after unequal third cleavage. G: 17-cell embryo, after subsequent cleavage. H: 22-cell embryo, showing trunk ectoderm precursor 2d111 (dark blue), trunk mesoderm precursor 4d (red), and endoderm precursors (purple); lateral pole view. I: Comparison of blastula fate maps of Oxydromus and Tubifex, as seen from left lateral view. A-D after Treadwell (1901) and Anderson (1973); E-H after Penners (1922) and Anderson (1973); I modified after Anderson (1973).
inherits the letter from their progenitor cell, but the animal blastomeres are designated by the lowercase letter corresponding to their quartet of origin, while the vegetal ones retain the capital letter designation; all get a number 1 in front. Thus, an 8-cell embryo has an animal quartet composed of micromeres la, lb, lc, and Id, and a vegetal quartet composed by macromeres 1A, IB, 1C, and ID (Figure 4.2B, F). After the fourth cleavage, the descendants of the micromeres retain the prefix 1, while the animal and vegetal descendants of the vegetal quartet get the prefix 2; for example, macromere ID generates an animal micromere and a vegetal macromere, designated 2d and 2D, respectively. As the micromeres divide, the animal-facing daughter of each micromere is distinguished by a superscript 1, and the vegetal- facing progeny gets a superscript 2. For example, the animal and vegetal daughter cells of blastomere Id are Id1 and Id2, respectively. Further divisions add another superscript 1 or 2, e.g., the daughters of Id2 are Id21 and Id22 (Figure 4.2C-D, G-H). In further rounds of division, descendants of the vegetal-most quartet of cells, the macromeres, keep incrementing their prefix, while progeny of the remaining cells increment their superscript as described earlier. This system, while somewhat cumbersome, provides a helpful framework that helps to trace the cell lineage for each cell of a 64-cell embryo, and to enable cell fate comparisons across species. On the other hand, the assumption that equivalently named cells are homologous can become problematic, for example, when evolutionary changes in cell division patterns or difficulties in catching certain divisions lead to ambiguity as to specific cell identities.
Comparisons of cleavage patterns across Annelida have shown both notable conservation and substantial deviations of the stereotypical pattern (Anderson 1973; Seaver 2014). In general, early development can be seen as a process that sequentially segregates cytoplasmic determinants—the molecular information that will eventually lead each cell and its progeny toward a specific developmental pathway. Such information might act in a cell-autonomous manner, or it might prime the cells to act in response to inductive interactions with other cells. Strategies to partition determinants differ across species, and the most obvious evidence is the equality or inequality in sister cell size at each cleavage. Cleavage equality is determined primarily by the amount and distribution of yolk, which in turn is strongly dependent both on the current life history strategy of each species, and the developmental biases imposed by the evolutionary history of its lineage.
-  It is important to note that the “dorsality” of D quadrant descendants is only true for even-numberedquartets (2d, 4d; Henry and Martindale 1998; Shankland and Seaver 2000).