Cellular and Molecular Mechanisms of Segmentation in Annelida

An Open Question

Eduardo E. Zattara and David A. Weisblat

CONTENTS

  • 4.1 Introduction to the Annelida...........................................................................71
  • 4.2 Segmentation in Annelids...............................................................................73
  • 4.3 An Overview of Annelid Development..........................................................75
  • 4.3.1 Early Embryonic Development...........................................................76
  • 4.3.2 Cell Fate Maps: Trochophore Larvae and Direct Development.........78
  • 4.4 Segmentation of the Trunk.............................................................................82
  • 4.4.1 Segment Development in Owenia......................................................84
  • 4.4.2 Segment Development in Platynereis dumerilii.................................85
  • 4.4.3 Segment Development in Capitella teleta..........................................87
  • 4.4.4 Segment Development in Tubifex tubifex...........................................88
  • 4.5 Molecular Basis of Annelid Segmentation.....................................................90
  • 4.6 Evolutionary Remarks....................................................................................92

References................................................................................................................93

Introduction to the Annelida

Annelida comprises a large and diverse set of worms inhabiting marine, freshwater, and terrestrial habitats. Most annelids share a stereotypical elongated vermiform body plan formed by a usually large number of repeated segmental units bound at the anterior and posterior ends by caps of terminal non-segmental tissues (Figure 4.1 A, C). They have a through gut, blood vessels, and repeated excretory organs running along the body, traversing a large coelomic cavity frequently compartmentalized by segmental septa. Their body wall is muscular, with variably thick bands of longitudinal muscle running along and finer rings of circular muscle, oriented transversal to the main body axis. Most species have segmentally iterated bundles of bristles that emerge directly from the body wall or from lateral appendages called parapodia. A ventral nerve cord runs from the posterior to the anterior end, where it is connected to a dorsal brain by pairs of nerves that go around the foregut.

Annelid body plan and developmental capabilities. A-В

FIGURE 4.1 Annelid body plan and developmental capabilities. A-В: Generalized adult (A) and larval (B) annelid body plans. A subterminal segment addition zone in the trochophore larva develops a posterior growth zone that intercalates segmental units between the terminal anterior (prostomium and peristomium) and posterior (pygidium) regions. C: Generalized body segment, as seen in clitellates. Abbreviations: cm, circular muscle; dbv, dorsal blood vessel; dc, dorsal chaetal sac; ep, epidermis; lm, longitudinal muscle; nph, metanephridium; pn, peripheral nerve; sep, septum; vbv, ventral blood vessel; vc, ventral chaetal sac; vg, ventral ganglion; vnc, ventral nerve cord. Polychaetes often bear their chaetae in lateral appendages called parapodia. D: Levels of regenerative ability (anterior and posterior) found across annelids. Regenerated tissues represented in green; growth zones shown in gray. E: Types of agametic reproduction by fission found in annelids. New tissues shown in green; growth zones shown in gray. A, D, and E modified after Zattara and Bely (2016); В modified after Nielsen (2005); C modified after Zattara and Bely (2015).

Although this basal body plan is well conserved across the phylum, several groups show significant divergence, to the point of completely losing the segmental organization, like sipunculans, echiurans, or orthonectids.

More than 18,000 annelid species have been described. Many of them serve important ecological roles, being key prey or predators, ecosystem engineers, or even unwelcome invaders (Brusca and Brusca 1990; Zhang 2013). Annelids are ancestrally marine; most marine segmented worms are usually referred to as poly- chaetes. Recent phylogenetic analyses support a number of annelid lineages (including Oweniidae, Mageloniidae, Chaetopteridae, Amphinomida, and Sipuncula) branching basally to two major clades: Errantia and Sedentaria (Struck et al. 2011; Weigert et al. 2014). Within Sedentaria arose a lineage that moved out of the sea into freshwater and terrestrial habitats. This group is known as the Clitellata, reflecting one of their adaptations to these novel environments. Clitellata diversified greatly, giving rise to a series of oligochaete lineages and the one giving rise to leeches (former class Hirudinea).

Most annelids reproduce sexually; several lineages have also evolved asexual reproduction (Schroeder and Hermans 1975; Zattara and Bely 2016). Most poly- chaete annelids have separate sexes; their gonadal tissue tends to be diffuse and spread out along the body. Males and females gather to spawn, and fertilized eggs develop indirectly into a variety of larval forms: planktotrophic larvae feed on other organisms in the plankton; lecithotrophic larvae continue development nourished by yolk inherited from the egg. Eventually most larvae metamorphose and settle down, adopting a more benthic habit. Different lineages have evolved a diversity of parental care strategies, like brooding in pouches or tubes, or provisioning of nurse eggs. For example, the lineage leading to the Clitellata evolved a suite of strategies to adapt to freshwater and terrestrial environments, including hermaphroditism, internal fertilization, laying their eggs within a protective cocoon secreted by a specialized epidermal band, the clitellum, and direct development of the eggs to hatch small juveniles. Correlated with these traits, gonadal development in clitellates became restricted to a few specific segments of the body.

Many annelid species also exhibit agametic asexual reproduction by fission to quickly increase their numbers. There are two main modes of fission (Figure 4.1E): In architomic fission, a worm fragments itself into two or more pieces; each piece then regenerates any missing body part resulting in a completely functional worm. In par- atomic fission, the development of new anterior and posterior regions within the axis of the parental animal precedes physical separation of the daughter individuals. Despite the heterochronic difference in development and separation between architomy and paratomy, both modes of fission rely heavily on developmental processes associated with regeneration (Figure 4. ID), and most likely represent a co-option of regeneration for reproductive purposes (Chapter 10; Zattara and Bely 2011, 2016).

 
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