Cell Fate Maps: Trochophore Larvae and Direct Development

In the context of our current knowledge of annelid phylogeny (Struck et al. 2011; Weigert et al. 2014), indirect development with an intermediate trochophore larval form is considered the ancestral mode for this phylum. A stereotypical trochophore (Figure 4.1B) is spheroid to fusiform in shape, with its long axis aligned with the embryonic anteroposterior (or animal-vegetal) axis (Rouse 2006). A characteristic ciliated band called the prototroch encircles the larva at an approximately equatorial position. Tissues anterior to the prototroch form the episphere and develop initially as larval epithelium and organs (in species with little yolk and plankton-feeding larvae) or directly as adult prostomial tissues (in species with larger, yolkier embryos and more abbreviated development). The mouth is usually located midventrally, posteriorly adjacent to the prototroch. Sometimes a second ciliated band called metatroch is located at a subequatorial position. Tissues posterior to the prototroch/metatroch form the hyposphere, which often bears a second, smaller and subterminal ciliated band known as the telotroch, and a longitudinal ciliated band running along the ventral midline from the mouth to the telotroch known as the neurotroch. Additional bands of ciliated cells are present in some groups; however, no lineage has a larval form possessing all known types of bands (Rouse 2006). The hyposphere becomes incorporated into the adult pygidium (Figure 4.1A-B).

The animal-most quartet of cells, descended from the primary micromere quartet (that is, cells la1, lb1, lc1, Id1) develop to become the episphere and part of the prototroch, while their vegetal sister cells (la2, lb2, lc2, Id2), together with the second micromere quartet (2a, 2b, 2c, 2d) contribute to the prototroch, post-trochal ectoderm, and larval muscles (Figure 4.21, Figure 4.3). In most species, all trunk ectoderm will derive from descendants of 2d, while all trunk mesoderm is derived from cell 4d in the fourth micromere quartet (Figure 4.3). Several major groups present slight to extreme deviations from this generic pattern (Meyer et al. 2010), but an important aspect to keep in mind is that a large proportion of the initial set of blastomeres are fated to build the component tissues of the trochophore. In turn, most of the trochophore (i.e., tissues located anterior to the telotroch) will be either reabsorbed or become part of the prostomium, the anterior, non-segmental terminal region of the adult worm. Larval tissues posterior to the telotroch develop into the pygidium, the posterior, non-segmental terminal region of the worm (Nielsen 2005). Thus, most of the body of an adult, indirect-developing annelid—the segmented trunk—is composed of tissues derived from a very small fraction of the initial embryonic blastomeres (Figure 4.21, Figure 4.3).

Trochophore larvae eventually metamorphose into juvenile worms; the degree of morphological change involved in this process varies depending on the life history strategies of each species and group. Along with ecological changes associated to shifts in habitat and/or feeding mode, metamorphosis is made evident by the developmental activation of the segmental region of the body, which effectively converts a spheroidal larva into a long, segmented worm (Figure 4.4). This growth by addition of segments is achieved through the proliferative activity of a PGZ (Figure 4.1 A-B). This PGZ derives from a ring of ectodermal stem cells (termed ectoteloblasts) enclosing a pair of large mesodermal stem cells (the M cells), just in front of the telotroch (Anderson 1973). In groups where unequal cleavage leads to large 2D and 2d blastomeres, this ectoteloblast ring derives from descendants of the 2d blastomere; when 2d is relatively small, progeny of 3c and 3d also contribute to this region. In most groups, equal division of the 4d cell of the fourth quartet along a parasagittal plane generates the pair bilateral of M cells, also known as mesoteloblasts. Together, the ectoteloblasts and the mesoteloblasts will proliferate to form segmental tissues (see next section).

Among indirectly developing groups, variation in the amount of egg yolk and larval ecology correlates with both the initial size of the ecto- and mesoteloblasts, and the timing of production of segmental tissues. Planktotrophic larvae (e.g., Owenia, Chaetopterus) developing from small eggs usually show smaller teloblasts with little

Comparison of embryonic cell fates between Platynereis dumerilii (Errantia

FIGURE 4.3 Comparison of embryonic cell fates between Platynereis dumerilii (Errantia: Nereidae), Capitella teleta (Sedentaria: Capitellidae), and Tubifex tubifex (Clitellata: Naididae). Ectodermal fates are indicated in blue (dark blue for trunk ectoderm, light blue for other ectoderm), mesodermal fates in red (red for trunk mesoderm, pink for other mesoderm), and endodermal fates in purple.

Developmental diversity of annelids. A-В

FIGURE 4.4 Developmental diversity of annelids. A-В: Protrochophore (A) and metatrocho- phore (B) stages of Oweniafusiformis; notice the developing segmented trunk in B. C-D: Larval L2 (C) and L4 (D) stages of Chaetopterus sp. E-F: Metatrochophore (4.5 days old) (E) and nec- tochaete (9 days old) (F) larvae of Nereis pelagica. G-H: Protrochophore (G) and metatrochophore (H) stages of Capitella sp. I—J: Gastrulating (I) and germband (J) stages of embryos of Tubifex tubifex. Abbreviations: ae, adult eye: an, anus: at, apical tuft; ch, chaetal bundle; ec, ecto- teloblast; ey, larval eye; gb, germband; Is, larval segment; mg, midgut; mo, mouth; ms, mesotelo- blast; pt, prototrochal band; ts, trunk segment; tt, telotrochal band; ys, yolk sac. Drawings not to scale. A-В and G-H after Lacalli (1980); C after Wilson (1883); D after Irvine etal. (1999); E-F after Wilson (D. P. Wilson 1932b); I after Penners (1924); J after Anderson (1973).

to no developmental activity during early larval life; activity resumes after larva begins to feed. In contrast, lecithotrophic larvae (e.g., Platynereis, Capitella) developing from larger, yolkier eggs tend to show larger teloblasts that initiate segment formation sooner. In many groups, three or more segments form before metamorphosis; in many cases, these initial segments are specialized for larval function. They develop very quickly, often almost simultaneously, and show ectodermal segmentation before any signs of mesodermal segmentation (in contrast to normal segmental development, see later). Upon metamorphosis, formation of segments is resumed, this time at a slower pace and showing a clearer anteroposterior sequential progression. These differences can be explained by heterochronic adjustments in the developmental timing of ectodermal and endodermal metamerism, relative to each other and to metamorphosis. Presence of larval segments varies not only across larger annelid taxa, but also among closer relatives that vary in their larval life history strategies (Akesson 1967). Such lability demonstrates the flexibility of spiralian development to support adaptive changes in the ecology of a lineage.

A more dramatic demonstration of the flexibility of annelid development and the role of heterochronic adjustments is seen in the direct development of Clitellate annelids (e.g., Tubifex). In this group, the larval stage is completely omitted, and segment development starts early in development from very large teloblastic precursors (see later and Chapter 7). Interestingly, even though this group comprises both species with large, yolky eggs and species where yolk has been reduced and feeding switched to albumen, cleavage leads to blastulae sharing a similar basic pattern: a large dorsal 2d cell or equivalent that gives rise to presumptive ectoderm, a similarly large 4d cell or equivalent that gives rise to presumptive mesoderm, an arc of micro- meres dorsal and anterior to the 2d cell that will form presumptive stomodaeum, and a set of larger vegetal cells that will become presumptive midgut (Figures 4.21 and 4.3). Such convergence is reached by different adaptations of the cleavage pattern in each lineage to deal with the reduction of yolk and the switch to albumenot- rophy (i.e., embryogenesis driven by albumen reserves within the egg cocoon and yet external to the embryo itself), and greatly illustrates both the evolutionary plasticity of early development and the high conservation of specific embryonic stages.

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