Embryonic and post-embryonic development of the polyclad flatworm Maritigrella crozieri; implications for the evolution of spiralian life history traits

Abstract

BackgroundPlanktonic life history stages of spiralians share some muscular, nervous and ciliary system characters in common. The distribution of these characters is patchy and can be interpreted either as the result of convergent evolution, or as the retention of primitive spiralian larval features. To understand the evolution of these characters adequate taxon sampling across the Spiralia is necessary. Polyclad flatworms are the only free-living Platyhelminthes that exhibit a continuum of developmental modes, with direct development at one extreme, and indirect development via a trochophore-like larval stage at the other. Here I present embryological and larval anatomical data from the indirect developing polyclad Maritrigrella crozieri, and consider these data within a comparative spiralian context.ResultsAfter 196 h hours of embryonic development, M. crozieri hatches as a swimming, planktotrophic larva. Larval myoanatomy consists of an orthogonal grid of circular and longitudinal body wall muscles plus parenchymal muscles. Diagonal body wall muscles develop over the planktonic period. Larval neuroanatomy consists of an apical plate, neuropile, paired nerve cords, a peri-oral nerve ring, a medial nerve, a ciliary band nerve net and putative ciliary photoreceptors. Apical neural elements develop first followed by posterior perikarya and later pharyngeal neural elements. The ciliated larva is encircled by a continuous, pre-oral band of longer cilia, which follows the distal margins of the lobes; it also possesses distinct apical and caudal cilia.ConclusionsWithin polyclads heterochronic shifts in the development of diagonal bodywall and pharyngeal muscles are correlated with life history strategies and feeding requirements. In contrast to many spiralians, M. crozieri hatch with well developed nervous and muscular systems. Comparisons of the ciliary bands and apical organs amongst spiralian planktonic life-stages reveal differences; M. crozieri lack a distinct ciliary band muscle and flask-shaped epidermal serotonergic cells of the apical organ. Based on current phylogenies, the distribution of ciliary bands and apical organs between polyclads and other spiralians is not congruent with a hypothesis of homology. However, some similarities exist, and this study sets an anatomical framework from which to investigate cellular and molecular mechanisms that will help to distinguish between parallelism, convergence and homology of these features.

Ins and outs of Spiralian gastrulation

“…The primary motive force is in the germinal bands. This was demonstrated in cases where the micromere cap was experimentally reduced, in which it could be seen that Smith et al, (1996) Rawlinson (2010). (K-L) Live fluorescent images of the snail Crepidula fornicata during early stages of gastrulation by epiboly.…”

“…Epiboly is seen in the clitellate annelids Helobdella (Smith et al, 1996;Fig. 3 H-I) and Tubifex (Shimizu, 1982), the polychaetes Capitella (Boyle and Seaver, 2008 ; and Platynereis (Fischer et al, 2010), the echiuran Bonellia (Pilger, 1997), the spiunculan Themiste , polyclad flatworms including Imogine (Younossi-Hartenstein and Hartenstein, 2000) and Maritigrella (Rawlinson, 2010;Fig. 3J), the gastropods Crepidula (Conklin, 1897;Fig.…”

“…Both extremes are seen in two major groups of spiralians, the annelids and molluscs. Gastrulation by epiboly is probably ancestral for platyhelminths, and gastrulation via invagination is likely ancestral for nemerteans (Wada, 1985;Rawlinson, 2010). Thus, a key question might be: is direct, or indirect, development ancestral for the spiralians, and bilaterians at large?…”

“…In polyclad flatworms, the 1st-3rd quartet micromeres form an irregular double-layered micromere cap (Fig. 3J), with the ectomesoderm already internalized prior to the beginning of epiboly (Younossi-Hartenstein and Hartenstein, 2000;Rawlinson, 2010). In Imogine, although the internalization of these ectomesodermal cells could not be determined definitely, mitotic figures were never seen to be perpendicular to the surface as this cap proliferated, suggesting that either the ectomesodermal cells are born to the interior very early, or they delaminate prior to, and during, epiboly.…”

Sipuncula: an emerging model of spiralian development and evolution

“…Observations from quartet spiral-cleaving embryos show that both equal and unequal cleavage patterns are found among mollusks and annelids (see Lambert, 2010). However, equal cleavage is the only pattern observed in the embryos of polyclad turbellarians (Surface, 1907;Boyer and Henry, 1998;Rawlinson, 2010), nemerteans (Martindale and Henry, 1995;Henry and Martindale, 1998;Maslakova et al, 2004), and echiurans (Torrey, 1903;Newby, 1932). This shows that equal cleavage appears to be common, as well as a 'fixed' pattern in three distinct spiralian lineages, and perhaps more.…”