Morphallactic Processes

Although the generic annelid body plan is built upon relatively similar segmental units, many groups show regional differentiation along the main body axis. Some tube-building species like chaetopterids or sabellids have strongly marked differences between different sets of segments, forming regions termed “tagmata,” a term borrowed from arthropod morphology. But more subtle differences in gut regionalization, nervous system organization and gonadal distribution can be found even in groups showing much more segmental homogeneity (Takeo, Yoshida-Noro, and Tochinai 2008; Zattara and Bely 2015; Jong and Seaver 2016). The process of regeneration restores the non-segmental terminal regions and a limited number of segments. When the regenerated segments are fewer than those removed by amputation, a positional mismatch between the proximal new segment and the stump results. This mismatch is usually solved by remodeling the old tissue into the morphology that corresponds to its new positional identity, a process known as morphallaxis.

Morphallaxis ranges from striking changes in overall morphology seen during the transformation of abdominal segments to thoracic segments in sabellids (Berrill 1978), to quite subtle changes associated with remodeling the gut in the clitellates Pristina leidyi and Enchytraeus japonensis (Takeo, Yoshida-Noro, and Tochinai 2008; Zattara and Bely 2011) or the ventral nerve cord in Lumbriculus variega- tus (Drewes and Fourtner 1991; Martinez, Menger III, and Zoran 2005; Martinez, Reddy, and Zoran 2006).

In the sabellid Sabella pavonina, the anterior 5-11 thoracic segments have dorsal bristles and ventral hooks, while the remaining abdominal segments have ventral bristles and dorsal hooks. Upon amputation at the abdominal region and formation of an anterior blastema, segments closest to the wound site lose their bristles and hooks and redevelop them in reversed position 2 or 3 days later. This morphallactic process proceeds in anteroposterior steps and finishes in the last affected segment about the time that anterior regeneration is complete (Berrill and Mees 1936).

In the clitellate Pristina leidyii, the gut forms a stomach-like bulge at segment 7. After amputation at a position posterior to that position, anterior regeneration restores only four segments; thus, during anterior blastema formation and development, the gut within the three segments adjacent to the wound site loses cilia and adopts a stomach-like morphology at the third segment from the original amputation plane (Zattara and Bely 2011). A similar process occurs in another clitellate, Enchytraeus japonicus; in this species, expression of three genes (a-tubulin, mino, and horu) localizes to specific regions of the gut, and amputation causes initial downregulation of all three genes, followed by upregulation that reestablishes the normal expression pattern in each regenerating fragment, and consequent morphallactic changes in the gut morphology (Takeo, Yoshida-Noro, and Tochinai 2008).

Morphallactic changes in the gut, blood vessels, and nephridia have also been reported for the clitellate Lumbriculus variegatus (Berrill 1952). In this species, morphallaxis of the ventral nerve cord at both functional and molecular levels has been reported. Electrophysiological measurements following amputation have characterized rapid shifts in the anteroposterior range of the sensory fields mediating fast escape responses (Drewes and Fourtner 1991). Regeneration also induces changes in the expression of neural proteins associated with shifts in positional identities and neurobehavioral plasticity (Martinez, Menger III, and Zoran 2005).

Morphallactic adjustments of the ventral nerve cord have also been evidenced by reorganization of the expression domains of Hox genes during posterior regeneration in Alitta virens and Capitella teleta (Novikova et al. 2013; Jong and Seaver 2016). In both species, amputation of posterior fragments causes a forward shift in the anterior expression boundary of lox4, lox2, and Post2. While in Alitta several other hox genes also adjust their expression domains, in Capitella most Hox gene expression remains stable after amputation. This might be explained by different deployment strategies for these genes among the two species: in nereids (Alitta and Platynereis) Hox genes are expressed in overlapping domains with variable anterior boundaries and a common posterior boundary located at the posterior growth zone, whereas in Capitella most of these genes have overlapping expression domains comprising the anterior, thoracic segments, with staggered anterior and posterior boundaries (Jong and Seaver 2016). Such differences in how Hox genes are used to specify body regions within the same body plan highlight the concept that developmental genes belong to a toolkit, and strategies for their deployment, while usually conserved, are not fundamentally constrained and can evolve in different directions.

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