Clonal domains in postlarvalPlatynereis dumerilii (Annelida: Polychaeta)

Abstract

Following an enzymatic procedure for softening the egg envelope, blastomeres in the embryo of the polychaete Platynereis dumerilii were injected with TRITC-dextran. Injection was successful in the following blastomeres: AB, CD, A, B, C, D, 1a-1d, 1A-1D, 4d, and 4d(1). The distribution of fluorescent label was recorded by confocal laser scanning microscopy of young, three-segmented worms after 3 or 4 days of development, in some cases also in 1-day-old trochophore larvae. Results were documented by single optical sections, by stacking a limited number or a complete set of optical sections, and by computer-generated surface views of both the labeled tissue domains and the body contours from complete image stacks of whole worms. With respect to their descent from the embryonic cell pattern, five major compartments can be distinguished which together compose the body of the young worm: 1) The epispheric, epidermal, and neural region of the head, composed of four domains arranged as quasi-radial sectors derived from micromeres 1a, 1b (left and right ventral), and 1c and 1d (right and left dorsal). 2) A posttrochal epidermal region of the head originating from micromeres 2a(1)-2c(1) and constituting the ventral and lateral posttrochal epidermis of the head. 3) A stomodeal-ectomesodermal region of the head, including the stomodeum (micromeres 2a(2) and 2c(2)), its mesodermal envelope, and head mesoderm (micromeres 3a-3d). 4) A solid cone composed of the four terminal macromeres 4A-4D, forming the core of the trunk as the endoderm anlage. 5) An epidermal and mesodermal coating of the trunk originating from the dorsal micromeres 2d and 4d. The region of the so-called (first, anterior) peristomial cirri at the posterior flanks of the head is also composed of 2d- and 4d-derived trunk tissue, thus corroborating the postulated descent of this region and its appendages from a cephalized anteriormost trunk segment and its parapodia. The cell-lineage domains of the first and third micromere tiers are arranged left or right of the sagittal plane, while two micromeres of the second quartet are in a lateral and, initially, two in a median position (2b ventral and 2d dorsal). The offspring of micromere 2d expand from a dorsal position toward the ventral midline and those of cell 4d from a posterior-dorsal site toward the anterior, initially forming two lateral bands. In the epispheric part of the head, part of the neurectodermal tissue derived from micromeres 1a and 1b interweaves in a medio-sagittal bar, and part of the first micromere offspring of all four quadrants (1a-1d) combine in forming a central brain neuropil. Each of the latter sends neurites through both of the circumesophageal connectives. Paired muscle tracts extend through the head toward the base of the antennae and are probably derived from micromeres 3a and 3b. A mesodermal envelope of the stomodeum is probably built by the 3c and 3d micromeres. The formation of symmetry and the nature of the body axes in the embryo and adult of Platynereis dumerilii are discussed....

Segment formation in Annelids: patterns, processes and evolution

“…This has not been resolved unambiguously in Platynereis to date. Lineage tracings of blastomere fates with diI in cleavage-stage embryos of Platynereis have been carried out up to three days of development (Ackermann et al, 2005). Injection of the 4d blastomere, which belongs to a homologous lineage to the leech DM blastomere labels the whole trunk mesoderm of the larva but more heavily labels a small group of cells located internally just in front of the forming pygidium.…”

Variation in spiralian development: insights from polychaetes

“…A second technique, called 4D microscopy, utilizes time-lapse imaging to follow individual cells using a semi-automated cell tracking system . This methodology requires optically clear embryos and gives detailed cell division information, but there is limited or no of the fate map were inferred by subtractive logic (Ackermann et al, 2005). A second Platynereis study utilized 4D microscopy to examine cleavage patterns (Fischer and Arendt, 2013).…”

“…In polychaetes, there are only four modern cell lineage or fate mapping studies published to date, including two studies each for Capitella teleta and Platynereis dumerilii (Ackermann et al, 2005, Fischer and. In one Platynereis study, identified blastomeres were microinjected for a limited set of blastomeres (1 st quartet micromeres, 1 st quartet macromeres, 2d 112 , 4d and 4d 1 ), and several features B C A Spiralian development in polychaetes 461 (Eisig, 1899), although his results were received with skepticism by his contemporaries (Nelson, 1904, Treadwell, 1901.…”

Cell Proliferation Pattern and Twist Expression in an Aplacophoran Mollusk Argue Against Segmented Ancestry of Mollusca

“…Yet, in mollusks, the mesodermal bands have generally been described as mostly less extensive and rather short lived, especially when compared to the situation in annelids (Korschelt and Heider, 1936; Raven, 1966; Fioroni, 1971, 1992; Wanninger and Wollesen, 2015). In the worm‐shaped solenogasters, however, the mesodermal bands seem to acquire larger dimensions and persist for a considerable period of time–a condition, which is more similar to other spiralians, especially annelids (e.g., Mead, 1897; Schmidt, 1925; Okada, 1940; Anderson, 1959, 1966, 1973; Goto et al., ’99; Ackermann et al., 2005; Seaver et al., 2005; Dill et al., 2007; Woodruff et al., 2007; Fischer and Arendt, 2013). Furthermore, the situation we observed is in agreement with classical descriptions on mesoderm formation and differentiation of solenogasters and polyplacophorans (Pruvot, 1890, 1892; Heath, 1899; Naef, 1924; Hammarsten and Runnström, 1925; Baba, 1938; Thompson, 1960; Salvini‐Plawen and Bartolomaeus, 1995) but is demonstrated here for the first time over the entire course of development using state‐of‐the‐art techniques.…”