Evolution of the bilaterian body plan: what have we learned from annelids?

Abstract

Annelids, unlike their vertebrate or fruit fly cousins, are a bilaterian taxon often overlooked when addressing the question of body plan evolution. However, recent data suggest that annelids offer unique insights on the early evolution of spiral cleavage, anteroposterior axis formation, body axis segmentation, and head versus trunk distinction.

Figure 1

Annelids and a number of other lophotrochozoans manifest a conserved pattern of early development known as spiral cleavage. (A) The first two cleavage planes fall at right angles parallel to the animal–vegetal axis and divide the zygote into the A, B, C, and D quadrants. In some but not all spiralians, the D blastomere is larger than the rest. Beginning with the third round of cleavage, the A, B, C, and D blastomeres cleave off (arrows) quartets of smaller cells called micromeres at the animal pole. Micromeres are colored according to quadrant of origin, with color intensity differing for odd- and even-numbered quartets. In spiral cleavage, each quartet of micromeres is rotated with respect to the parent blastomere, and the chirality of rotation alternates for odd- and even-numbered quartets. (B) Embryonic fate map of the nemertean Cerebratulus (adapted from ref. 4). Clones derived from the four B quadrant micromeres (cyan) and D quadrant micromeres (red) are numbered. Note that odd- and even-numbered quartets have distinct symmetry properties, with the odd-numbered micromeres being rotated 45° clockwise as viewed from the animal pole. Thus, in the first and third quartets, the A and D quadrants are on the left, bilaterally symmetrical to the B and C quadrants on the right. Only the second and fourth quartets have the “traditional” spiralian fate map (1), with D being dorsal and B ventral. (C and D) Although ignored for many years, the alternating symmetry of the spiralian fate map is readily apparent in the tracings of early annelid embryologists. C is an adaptation of R. Woltereck's (30) tracing of the polychaete annelid Polygordius nearing the end of gastrulation. Thick outlines demarcate clones derived from single micromeres. Clones derived from the five B quadrant micromeres (cyan) and D quadrant micromeres (red) are numbered, and it can be seen that the plane bisecting the B and D quadrants is rotated by 45° for odd- and even-numbered quartets. Part D is an adaptation of E. B. Wilson's (2) tracing of the polychaete annelid Nereis at a similar stage but seen from the animal pole. The animal hemisphere is composed of the four primary micromere clones (same color scheme as other figures), with the D lineage contributing to the left-dorsal quadrant. Also note that the second quartet micromere from the D lineage (primary somatoblast) straddles the dorsal midline. The primary and secondary somatoblasts (second and fourth quartet micromeres from the D lineage) are the main source of ectoderm and mesoderm in the adult spiralian body plan, and in Nereis, these cells are larger than the other micromeres. The symmetry properties of these two even-numbered micromeres became an all-encompassing tenet of spiralian embryology (i.e., D is dorsal) for most of the 20th century, and it is only with the advent of modern cell-labeling techniques that the true complexity of the spiralian fate map has been rediscovered (–8).

Figure 2

Expression of Hox genes in developing annelids shown by in situ hybridization. (A) In embryos of the leech Helobdella triserialis, expression of the Hox genes begins during organogenesis, long after the formation of segments and the specification of segment identity (10, 14, 15). Embryo is stained for expression of Lox2 (Hox paralogue group 7/8) and shown in ventral view with anterior to the top of the page. Lox2 RNA is detected only in the posterior two-thirds of the body plan, including intense staining in the ganglia of the central nervous system (solid arrow) and reproductive structures (hollow arrow) and faint staining in the segmental mesoderm. (B and C) The onset of Hox gene expression in larvae of the polychaete annelid Chaetopterus varieopedatus is coincident with the formation of segments and first appears in a posterior growth zone from which the differentiating segments emerge (11). Larvae are shown in dorsal view with anterior to the top of the page and an arrowhead marking the posterior pole. Gene expression is restricted to the posterior growth zone, on either side of the pole. B shows expression of gene CHv-Hox2 (Hox paralogue group 2), and C shows expression of gene CHv-Hox3 (Hox paralogue group 3). Images in B and C are courtesy of Steve Irvine and Mark Martindale (Univ. of Hawaii, Honolulu, HI).

Figure 3

Expression of the en gene does not seem to be required for the establishment of normal segment polarity in the leech Helobdella (ref. and E.C.S. and M.S., unpublished results). (A) The primary p blast cell gives rise to one segmental repeat of the leech's dorsolateral ectoderm. The en protein (shaded nucleus) is expressed in only one of the four granddaughters of the primary blast cell (21). ANT, anterior; POST, posterior. (B) Laser ablation of the en-expressing cell has no detectable effect on the specification of more anterior or posterior parts of that same blast cell clone. (C) Laser ablation of the anterior daughter of the primary P blast cell prevents the formation of the en-expressing granddaughter. This manipulation has no detectable effect on the specification of the posterior half of that same blast cell clone nor on the segment polarity of the next anterior blast cell clone. These results suggest that en-initiated cell interactions are not required for the proper specification of segment polarity in the leech.

Figure 4

Radial head model for the origin of the bilaterian body plan. (A) This model assumes a prebilaterian ancestor (orange) with a radially organized body plan and a single gut opening, shown here at the bottom. For convenience, the ancestral body plan has been divided into quarters, and a hypothetical gene expression domain is shown by shading. Transition to the modern bilaterian body plan began with the asymmetric specification of a specialized group of “trunk” precursor cells (cyan) at only one meridian around the circumference of the ancestral body plan. (B) Allometric expansion of the trunk domain produces a body plan typical of most Bilateria. The trunk elongates away from the head domain, carrying with it the anal end of a now bipolar gut. But the head domain retains features of its ancestral radial organization, as noted by a gene expression pattern (shaded) concentric around the mouth. This model proposes that bilaterian “head genes” have been relegated to the head domain, because they were not coopted into trunk patterning, and suggests that the AP axis may be an innovation of the Bilateria rather than a modification of a preexisting axis. [Reproduced with permission from ref. (Copyright 1998, Academic Press)].