Spatiotemporal Registration of Blast Cell Clones
The juxtaposition of parental (M, O, and P) lineages and grandparental (N and Q) lineages within the germinal bands of the Helobdella embryo presents a pair of fascinating conundrums regarding the spatial and temporal registration of blast cells that are destined to contribute to a given segment.
First, given that all the blast cell progeny are about the same size, one segment’s worth of cells in the n and q bandlets takes up twice as much space as one segment’s worth of cells in the m, o, or p bandlets as the cells enter the germinal band Figures
7.3 and 7.4). This initial spatial discrepancy is corrected as cells begin dividing, because the individual m, o, and p blast cell clones elongate to match the combined length of the neighboring f and s blast cell clones in the n and q bandlets. This positional correction is manifested by the continual movement of n and q bandlets relative to the m, o, and p bandlets at the posterior ends of the germinal bands (Weisblat and Shankland 1985).
A second puzzle arises from the observation that all the teloblasts divide at a rate that is roughly constant among teloblasts and throughout their production of segmental founder cells (Wordeman 1983). In Helobdella austinensis; the telo- blast cell cycle time is roughly 90 minutes at 23°C (Yoo and Bylsma, in preparation). All four subsets of teloblasts (M, N, О/P, and Q) begin making segmental founder cells at about the same time, at roughly 30 hours after zygote deposition (hrs AZD; leech embryos are fertilized internally but arrest at meiosis I until they are deposited into cocoons, so zygote deposition marks the onset of postfertilization development). Thus, the M and О/P teloblasts have made their entire complement of 32 segmental founder cells at about 78-80 hrs AZD. At this time, the N and Q teloblasts have also generated about 32 segmental founder cells, but these correspond to only 16 segments, and the N and Q teloblasts do not finish making 64 segmental cells each for another 2 days (148-150 hrs AZD; Yoo and Bylsma in preparation).
Put another way, leech embryos exhibit a progressive and segment-specific disparity in the age of consegmental blast cell clones—the blast cells from all segments that contribute to segment R1 are all born within a few hours of each other, but the n and q blast cells contributing to posterior segments are born more than a day later than the m, o, and p blast cells contributing to the same segments (bans et al. 1993). Moreover, so far as has been determined for Helobdella, each of the seven types of blast cell clones contributing progeny to a segment (m, nf, ns, o, p, qf, qs) develops according to an autonomous clonal clock rather than synchronizing their development to an external segmental clock (bans et al. 1993).
The temporal discrepancy between parental and grandparental lineages in Helobdella also raises questions concerning segmentation in oligochaetes, the paraphyletic annelid taxon from which leeches evolved (Erseus and Kallersjo 2004; Struck et al. 2011). So far as is known, the process by which segmental mesoderm and ectoderm arise during embryogenesis is well conserved among clitellate annelids, including the production of homologous, segmentally repeating M, N, О, P, and Q kinship groups from lineage-restricted, teloblastic stem cells and the same combination of parental and grandparental lineages as in Helobdella. An intriguing difference, however, is that whereas segmentation in leeches is a determinate process, many oligochaetes exhibit indeterminate growth and segmentation. That is, leeches produce their fixed complement of exactly 32 segments during embryogenesis, and with no post-embryonic segment formation. In contrast, many oligochaetes add somewhat indeterminate numbers of homonymous segments post-embryonically from a posterior growth zone (Zattara and Bely 2013; Bely et al. 2014). If oligochaetes maintain the same rules as leeches for producing segmental founder cells, with an increasing discrepancy between the birthdate of the N or Q versus M, О and P founder cell clones in posterior segments, it would suggest that posterior segments of mature specimens should be missing their N and Q kinship groups for substantial periods of time after the M, O, and P-derived cells have completely differentiated. Alternatively, it could be that post-embryonic segmentation in oligochaetes entails the emergence of new, more homogeneous stem cells, and/or that cell cycle times of post-embryonic segmentation stem cells are regulated differently than in the embryonic teloblasts.