In annelid species with indirect development—likely the ancestral mode for the phylum—embryonic development results in an unsegmented trochophore larva with a subterminal growth zone; segmental units form in front of this subterminal growth zone (see Chapter 4). As the larva metamorphoses into a juvenile, the growth zone keeps adding segments, resulting in a body plan that consists of a variable number of segmental units capped by two terminal regions. The anterior region derives from the larval tissues located anterior to the growth zone and comprises the prostomium and the peristomium. The posterior region derives from larval tissues located posterior to the growth zone and comprises the pygidium. Due to their larval origin, prostomium, peristomium, and pygidium are usually considered to be non-segmental in nature (but see Starunov et ah, 2015, for a differing view).
During axial regeneration, tissues from both the terminal cap and segments need to be reconstructed. In general, the terminal caps develop first from the regeneration blastema, and then segments arise and differentiate between the cap and the stump (Figure 10.2). A pattern of initial development of the distal portions of a regenerating structure, followed by intercalation of remaining structures, is seen during regeneration in many other systems outside annelids, and might reflect a common pattern of regenerative processes throughout animals (Agata, Saito, and Nakajima 2007).
Studies of intercalary regeneration of segments suggest this process is develop- mentally very similar to the addition of segments during normal growth (Gazave et al. 2013; Balavoine 2015; Ozpolat and Bely 2016). However, the rate of segment addition is usually much faster during regeneration, at least initially (de Rosa, Prud’homme, and Balavoine 2005; Niwa et al. 2013). The rate and extent of segmental regeneration varies widely across species (Berrill 1952). Marked differences in rate are also seen between posterior and anterior regeneration. In general, segments built during posterior regeneration show a clear developmental gradient where older segments are more anterior and farther away from the growth zone. During anterior regeneration, a similar gradient is seen clearly in some species (Allen 1923; Zattara and Bely 2011; Aguado et al. 2014; Weidhase, Helm, and Bleidorn 2015; Ribeiro, Bleidorn, and Aguado 2018); however, in other species, simultaneous development of all segments has been reported, leading to the suggestion that segment formation during posterior and anterior regeneration are fundamentally different processes (Balavoine 2015). Although near-simultaneous segment development can be explained by fast segment formation rates and relatively low numbers of anteriorly regenerated segments, a more accurate test of whether the process of segment addition differs between posterior and anterior regeneration will come from comparative studies of gene expression. Unfortunately, most species in which gene expression has been well characterized during regeneration are not capable of anterior regeneration (Kozin and Kostyuchenko 2015; Niwa et al. 2013; Zattara and Bely 2016; Jong and Seaver 2016; Planques et al. 2018). Thus, the answer will have to wait until gene expression studies are conducted on species capable of both anterior and posterior regeneration.