Segmentation in Annelids
The basic annelid body plan (see previous section) follows a clear pattern of segmental metamerism. Here, metamerism and segmentation are considered as two nested levels of organization. Metamerism, the more basic level, is defined as the organization of an animal body plan into repeating morphological units along the anterior-posterior (А-P) axis within any of the three germ layers (ectoderm, mesoderm, or endoderm). To rise to the level of segmentation, metamerism should meet two additional criteria: (1) morphological repeats should be present in two or more of the germ layers; and (2) repeats should have the same spatial frequency across layers. By this definition, metamerism is seen in a range of taxa including flatworms, mollusks, nematodes, onychophorans, and tardigrades (see Chapter 8), but segmentation is confined to annelids, arthropods, and chordates. The broad phylogenetic distribution of these body plan features has been interpreted in two ways. One is that metamerism or even segmentation was present at the base of the bilaterians and has been lost or modified in many different lineages. Alternatively, it could be that the ancestral bilaterian was neither segmented nor metameric, and that these features have evolved independently in various lineages.
Given the current level of knowledge in the field of evolutionary developmental biology (evo-devo), either of these scenarios may be true (Davis and Patel 1999; Patel 2003; Couso 2009; Chipman 2010). More important, in either case, the broad and phylogenetically intermingled distribution of non-metameric, metameric, and segmented body plans across the three superphyla of bilaterally symmetric animals (Deuterostomia, Ecdysozoa, Lophotrochozoa/Spiralia) calls for a much greater degree of evolutionary plasticity in developmental processes than was assumed to be the case when phylogenetic trees were constructed using morphological comparisons, as exemplified in the Articulata hypothesis (Scholtz 2002). In constructing such trees, segmentation often weighed heavily in organizing taxa, based on two assumptions: (1) that a segmented body plan would be difficult to evolve; and (2) that once evolved it would not be lost because of the selective advantages it confers. To more fully understand the evident evolutionary plasticity of developmental pathways leading to the gain or loss of segmentation and metamerism, it is necessary to compare axial growth and patterning among diverse models, including both segmented and unsegmented taxa representing different branches of the phylogenetic tree.
The phylum Annelida has traditionally been considered one of the three truly segmented phyla, the other two being the ecdysozoan Arthropoda and the deutero- stome Chordata. Several annelid groups, especially those more widely familiar to the general public like earthworms or lugworms, are often presented as the epitome of metameric organization: they have a long body composed of numerous, externally and internally similar compartments, and show little to no regional specialization, save for the terminal regions. Despite including some quintessential homonomously segmented groups, many annelids lineages show regional specializations grading from subtle differences of size and organ distribution along the anteroposterior body axis, to strong tagmatization similar to that seen in most arthropod groups. Furthermore, Annelida as currently understood based on molecular phylogenies (Struck et al. 2011; Weigert et al. 2014) also includes several taxa that show little to no trace of segmentation as adults, like peanut worms (sipunculans), spoon worms (echiurids), or beard worms and giant tube worms (siboglinids). The fact that traditional, morphologically driven phylogenies had classified these taxa as independent phyla, based in large part on their unsegmented body plans, is evidence of the evolutionary plasticity of developmental mechanisms in general and segmentation in particular. Thus, out of the “big three” truly segmented phyla, Annelida shows the largest diversity of evolutionary elaborations of the basic (perhaps, even ancestral) homonomously metameric body plan.
Another fundamental difference between annelid segmentation and that of arthropods and chordates is that segment development in annelids is not restricted to embryonic and larval development in most groups. Furthermore, segment number is usually variable, with segments forming throughout the whole life of the worms (see Chapter 7 for exceptions to these generalizations). In addition, many groups can replace lost segments by regeneration, and several can redeploy regenerative abilities during asexual reproduction. As such, annelid segment development can be considered the most robust yet flexible pathway to metamery among Metazoans.
Despite the undoubted relevance of annelid segmentation to our understanding of the developmental and evolutionary mechanisms leading to metameric organization in animals, we still know surprisingly little about its cellular and molecular underpinnings, relative to the state of knowledge in arthropods (Chapter 3) and chordates (Chapter 5). Most insights into how cells that will form segmental tissues are born and fated comes from studies on embryos of leeches, a specialized group within the clitellate annelids, which are already derived relative to their marine counterparts (Chapter 7). While what we have learned so far from leeches provides enormous insight into how cells can become segmental tissues, the mechanisms themselves are unlikely to adequately represent the segmentation mechanisms across most annelids, just as segmentation mechanisms described for Drosophila flies have been found to be quite distinct from those later found in other arthropod groups (Peel, Chipman, and Akam 2005). Fortunately, the last two decades have seen the emergence of new and powerful annelid models, spearheaded by the nereid Platynereis dumerilii and the capitellid Capitella teleta, which are likely to be followed by several other species with the help of the next generation of functional genomic tools and the rise of evo-devo approaches.