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For cross-comparison and presentation, we segmented out representative neurons via 3D interactive segmentation (Wan et al, 2021) and warped segmented neurons into the same standard fly brain through whole-brain alignment (Rohlfing and Maurer, 2003). To show single neurons with respect to hemilineage morphology, we created 25 hemilineage masks. The hemilineage masks of the seven lineages composed of dual viable hemilineages were generated by compiling representative A or B neurons of each type together.
In our limited survey, no replacement of any embryonic precursor by another was observed, but the postembryonic behaviour of two pairs of cells was found to be decided by regulative interaction in midembryogenesis. There is evidence for inductive effects upon morphogenesis, cell divisions, and cell deaths during the second half of embryogenesis. The period between the generation of the founder cells and the 50-cell stage has not yet been satisfactorily investigated.
Two cases of regulative interaction were found. Both occur in late embryogenesis and involve the confrontation of similar cells at the ventral midline, a situation which is already familiar from Postembryonic studies. In other respects the results are consistent with cell autonomous development, the evidence for autonomy being strong for the MS and late AB lineages. Interactions before the 50-cell stage are difficult to analyse by laser ablation.
We are also highly enthusiastic about the repeated nature of temporal fates as assessed by morphology. To examine this interesting phenomenon in a more systematic manner, we further compared the morphology of serially derived neuron types using NBLAST.
The head mesodermal cell (hmc) is more difficult to score, so the finding in this case was confirmed by watching for the death of its homologue. When MSapp or MSappa was ablated (three animals) the death was seen and hmc was absent from the larva; when MSppp or MSpppa was ablated (three animals) the death was not seen and hmc was present in the larva. Therefore, in spite of the similar embryonic appearance and position of hmc and its homologue, the latter is programmed to die even in the absence of the former.
Albertson, D. G, and Thomson, J. N. (1982). The kinetochores of Caenorhabditis elegans.
In the LALv1A hemilineage, there is serial innervation of various CX neuropils in the sequence of NO, EB, FB/NO, NO, then FB (with AB-targeting neurons at the end). Note the recurrent targeting of FB layers ([J] and [M]). The LALv1B hemilineage produces six morphological groups in oder, targeting IB, PS, SP, PLP, VLP, and PS again.
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The only novel finding pertains to that hemilineages with greater axon/dendrite coverage associated with the Noff state, implicating Non in inhibiting long-distance targeting. However, this idea is not tested functionally.
Klass, M, Wolf, N, and Hirsh, D. (1976). Development of the male reproductive system and sexual transformation in the nematode Caenorhabditis elegans.
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Nonetheless, we managed to examine the A/B morphological differences further with quantitative analysis per reviewer #2’s advice (see below for details). We now ascribe the A/B morphological distinctions primarily to the presence of multiple topological classes and/or morphological groups of B neurons as opposed to a single dominant group/class of A neurons (see second paragraph of Discussion). Our model has been therefore updated to propose that Notch suppresses neurite defasciculation and thus promotes joint neurite extension and neuropil innervation by A neurons (see third paragraph of Discussion).
The Postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans
Targeted cell-lineage analysis using lineage-restricted genetic drivers is therefore preferred for mapping specific neuronal lineages of interest with single-cell resolution (Awasaki et al, 2021). To date, only three of the about 100 distinct neuronal lineages have been fully mapped at the single-cell level in adult fly brains: the mushroom body (MB), anterodorsal antennal lobe (ALad1) and lateral antennal lobe (ALl1) lineages (Lee et al, 1999; Jefferis et al, 2001; Yu et al, 2021; Lin et al, 2021). These mapped lineages consist of 1) MB Kenyon cells (KC), 2) AL projection neurons (PN), and 3) AL/AMMC PNs and AL local interneurons (LN), respectively. All three lineages produce morphologically distinct neuron types in sequential order, indicating a common temporal cell-fating mechanism. However, the progeny’s morphological diversity varies greatly from one lineage to the next. The four identical MB lineages are composed of only three major KC types; moreover, paired KCs from common GMCs show no evidence for binary sister fate determination (Lee et al, 1999). By contrast, the two AL NBs produce progeny that rapidly change type (producing upwards of 40 neuron types) and the GMCs generate discrete A/B sister fates (Yu et al, 2021; Lin et al, 2021). In the ALl1 lineage, differential Notch signaling specifies PNs versus LNs (Lin et al, 2021). Notably, the paired PN and LN hemilineages show independent temporal-fate changes, as evidenced by windows with unilateral switches in production of distinct PNs or LNs (Lin et al, 2021). Moreover, the ALl1 PN hemilineage alternately yields Notch-dispensable AL and Notch-dependent AMMC PNs (Lin et al, 2021).
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Contrasting the complexity of early-born neurons, eight hemilineages (32%), SMPad1(A), SLPpm3(B), CREa1B, CREa2B, AOTUv1B, LALv1B, FLAa2(A), and VESa1(A), terminate with neurons that have drastically reduced domains of elaboration. Four of them, SLPpm3(B), CREa1B, FLAa2(A), and VESa1(A) (Figure 4), produce uniquely exuberant first larval-born neurons, then many neurons with intermediate elaboration, and lastly neurons with limited elaboration. Taken together, our data suggests that the extent of neuronal elaboration is negatively regulated by temporal fate in a similar manner across diverse lineages.
The final step in our analysis was to identify the surviving cells in terms of the known larval and adult anatomy. As many cells as possible were identified at 430 min (by comparison with serial section reconstructions of animals at this stage), because thereafter observation is much more difficult on account of movement of the embryo.
The dorsal hypodermal cells have very granular cytoplasm and form prominent transverse ridges. In figure 7 some licence has been allowed in depicting cell deaths, because of their importance in pattern recognition; in fact, they do not all become refractile simultaneously. WA editors' note: the positions of the descendants of Caaa and Cpaa are inadvertantly reversed in this fig (Loer C. et al, WBG 10(3)120).
Starting from the posterior dorsal side of the embryo, the cells spread anteriorly and posteriorly. The most posterior ones are body muscle precursors, which travel round to the ventral side and enter the interior immediately after D. Most of the remaining cells are employed in forming the dorsal hypodermis over the posterior two-thirds of the body; their nuclei migrate contralaterally (see Migrations).
The twin spots of each twin-spot NB clone were pseudo-colored the same to derive the whole full-size pattern (red). To account for the entire pattern (red) with a minimal number of single neurons (green), we merged one neuron per type or one neuron per subtype for types with obvious variations. Note extensive overlap between the green and red patterns, except in [L’] where an unrelated SEZ single-cell clone existed coincidently with the VESa2 twin-spot NB clone.
Figure 2I, K, L, M, N). By contrast, reduced affinity in B hemilineages could promote gross diversity through serial defasciculation of primary projections. Further, reduced affinity across sister branches could enhance neurite elaboration within targeted neuropils. In support of this model, Notch may directly act as a cell adhesion molecule or indirectly mediate cell adhesion through up-regulating canonical cell adhesion molecules such as integrins (Murata and Hayashi, 2021).
Robertson, A. M. G, and Thomson, J. N. (1982). Morphology of programmed cell death in the ventral nerve cord of Caenorhabditis elegans larvae.
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Zur Strassen (1959) based his conclusion -that in B. rigidum P4 yields the somatic gonad- upon the observations that P4 divides in the embryo and that the newly hatched larva contains only one germ cell. Although we were not able to obtain B. rigidum, we investigated another member of the order Tylenchida, Aphelencoides blastophthorus, which similarly contains a single germ cell at hatching. We find that P4 does not divide in the embryo of A. blastophthorus, and becomes the solitary larval germ cell. Comparison with the detailed drawings provided by zur Strassen (1892) shows that the early cleavages of the two nematodes are very similar and reveals the reason for the discrepancy: he had inadvertently reversed anterior and posterior, so that the dividing cell which he took to be P4 was in fact one of the AB group.
Brain neurogenesis involves conserved patterning mechanisms and employs homologous developmental genes across species (Huang, 2021; Vasconcelos and Castro, 2021). In Drosophila, a series of fating events must occur to promote neuron diversity. First, NBs acquire lineage identity via spatial patterning cues. Second, sequentially born GMCs inherit temporal factors. Finally, GMCs divide into pairs of distinct neurons, generating sister hemilineages with differential Notch signaling. Predetermined fates evidently guide most, if not all, aspects of neuronal differentiation in the invariant fly lineages (Erclik et al, 2021).
Note distinct temporal patterns of relatedness in diverse hemilineages. The CREa1B hemilineage displays progressive changes, and the SMPp&v1B hemilineage exhibits both progressive and cyclic changes. By contrast, the CREa2B and SMPp&v1A hemilineages yield more neuron types that appear in various cyclic manners. Please find the complete set of hemilineage NBLAST heatmaps in Figure 1—source data 1.
Descendants of the precursors enter the body cavity from the ventral side during late gastrulation. First to enter are the MS cells (120-200 min), next are the ABaraap cells (210 min), and last are the remaining AB cells (220-250 min). At first the dividing cells form a cylinder anterior to the intestine; gradually a distinct boundary appears at the surface of the developing pharynx; then, at about 400 min, it is compressed posteriorly and becomes almost spherical, but subsequently it gradually elongates, first anteriorly and then posteriorly. The transient compression coincides with a flux of anterior sensory neurons towards the tip of the head (see Nervous System) but the causal relationship between these events is unknown.
At 100 min after first cleavage, when the egg comprises 28 cells, gastrulation begins (figure 5). The first cells to enter the interior are Ea and Ep, which constitute the endoderm; they sink inwards from the ventral side, near the posterior end of the embryo. Next, at 120-200 min, are P4 and the progeny of MS. The entry zone widens and lengthens, spreading first posteriorly as most of the remaining myoblasts (derived from C and D) enter (180-230 min), and then anteriorly as the AB-derived part of the pharynx enters (210-250 min). The ventral cleft closes from posterior (230 min) to anterior (290 min). As gastrulation proceeds, the clone of E cells and the precursors of the pharynx form a central cylinder, while the body myoblasts insinuate themselves between this cylinder and the outer layer of cells. Although most of the myoblasts enter the body cavity during gastrulation, two do not. These are ABp(l/r)pppppa, which do not sink inwards until the time of their terminal divisions at 290 min.
Representative ALv1 neuron types (Non green) arranged in birth-order, shown in the context of all identified ALv1 neuron types merged together (grey). Note several recurrent features, including mono-glomerular AL innervation (B, C, E, F, I, K, M and N), extension beyond LH (D, H and P), and SEZ targeting (A, L).
Caenorhabditis elegans (Bristol), strain N2, was maintained according to Brenner (1974). Turbatrix aceti and Aphelencoides blastophthorus were kindly given to us by David Hooper, Rothamsted Experimental Station, Harpenden, Herts, England; Panagrellus redivivus was obtained from Rothamsted in 1976, and is the strain studied by Sternberg and Horvitz (1981, 1982). T. aceti and P. redivivus were maintained in the same way as C. elegans; A. blastophthorus was grown on NGM plates infected with mixed fungi.
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Figure 12. Schematic longitudinal section to illustrate cells and syncytia forming surface coverings of newly hatched L1. Part of the digestive tract is dotted to indicate that boundaries are not shown; for details of this region see Albertson and Thomson (1976) (pharynx) and figure 17 (remainder). Inset (above) indicates three-dimensional arrangement in central region; the four longitudinal grooves between hypodermis and intestine are occupied by body muscle. Commas indicate two cells meeting in plane of drawing. During postembryonic development: hyp7 enlarges (by fusion) into the P-cell region; in the hermaphrodite a vulva is formed and Y becomes a neuron; in the male there are extensive changes in the tail (Sulston and Horvitz, 1977; Sulston et al, 1980).
To analyze Vnd+ NBs, we created a GAL4 driver under the control of endogenous vnd regulatory sequences using gene targeting (Chen et al, 2021). To immortalize the NB expression of Vnd into the neuronal progeny, we derived a Vnd-specific, lineage-restricted LexA driver using a cascade of site-specific recombinases. This cascade is triggered by vnd-GAL4, filtered through dpnEE (a pan-NB promoter), and then driven ubiquitously so that each of the NB’s daughter cells express LexA (Figure 1A). To isolate/identify individual Vnd lineages, we utilized stochastic clonal induction of a conditional LexA reporter.
The large number of programmed cell deaths, and their reproducibility, is evident from the lineage. The most likely reason for the occurrence of most of them is that, because of the existence of sublineages, unneeded cells are frequently generated along with needed ones (Sulston and Horvitz, 1977; Horvitz et al, 1982).
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The AOTUv4A hemilineage, like LALv1A, produces only FB-targeting neurons after a short stretch of earlier larval-born non-FB neurons (Figure 10A–L). The FB neurons from AOTUv4A and LALv1A are remarkably similar, in both distal and proximal elaborations despite the fact that AOTUv4A targets FB layers 4–8, whereas LALv1A targets all FB layers. We also see similar recurrent targeting of some FB layers in both AOTUv4A and LALv1A hemilineages. Further, the first AOTUv4A FB neuron type exhibits interesting morphological features which are characteristic of the last LALv1A FB neuron type—both show similarly restricted dense elaborations in the SP as well as concentrated FB innervations in small subdomains on either the top (AOTUv4A) or bottom (LALv1A) of the FB (Figures 10B and 7Q). In conclusion, AOTUv4A and LALv1A make similar FB neurons in comparable temporal patterns.
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For example, in subsection “Neurons of same hemilineage origin vary in topology” to say that for the nomenclature "typically" or "we may add", is not best practice. The data should be released with a consistent nomenclature that is the same for all neuron types, and is objective, things like "main arborisation neuropile" can be subjective, instead things like first or last arborisation neuropile might be more appropriate. It would indeed be best to discuss with VFB what the most appropriate nomenclature might be.
CREa2B and SMPp&v1A in Figure 12E). Given NBLAST’s superb ability to detect local similarities, the widespread phenomenon of cyclic increases in similarity scores indicates the presence of recurrent morphological features. This aligns well with the insights we made above with manual analysis. Taken together, multiple hemilineage-characteristic features may recur at different frequencies to expand the morphological diversity of neurons in a combinatorial manner.
Custom algorithms were used to present the birth time of neuron types or morphological groups with heatmaps. The neuron-type heatmaps show manually sorted neuron types with actual single-cell numbers (max = 10) recovered from induction at given time points. The birth-order of neuron types was determined to our best judgement, based on relative time of beginning, ending, or peak recovery using both single-cell and NB clone data. By contrast, the morphological-group heatmaps show computer-sorted morphological groups that often consist of types made in discrete time windows.
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Note multiple recovery windows for LAL (I,L,O) and PS1 (J,P) groups. Tilted views at a lower magnification are showed to the right; anterior (A) to the left, posterior (P) to the right.
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Neurons and supporting cells other than those in the pharynx: White et al, (in preparation). This system is largely self-explanatory (see Appendix), but note that it uses symmetry operators as suffixes to distinguish cells which differ only in position (A, anterior; P, posterior; D, dorsal; V, ventral; L, left; R, right).
We will deposit the segmented neurons into Virtual Fly Brain upon acceptance of the paper. We indicate this plan of data sharing under the section of Data Availability.
There is some similarity between the intestino-rectal valve and the pharyngo-intestinal valve: in both, the intestine attaches to a ring of two cells which do not bear microvilli, which attaches in turn to a ring of three cells which do bear microvilli. Only the intestino-rectal valve is a true valve, in that it can be closed actively by means of a sphincter muscle which surrounds it.
The Embryonic Cell Lineage of the Nematode Caenorhabditis elegans
Extension of these experiments to MS(a/p) leads to pharyngeal damage, as predicted from the lineage. Not surprisingly, these animals feed poorly or not at all. Detailed analysis, which would require electron microscopical reconstruction, has not been undertaken.
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It subsequently turns to lie obliquely and acquires a twofold rotational axis of symmetry. This behaviour can be understood if, during late embryogenesis, the two subunits interact specifically with one another but not with nongonadal tissues, the oblique position being a consequence of packing. The autonomy of the gonad was pointed out by Kimble and Hirsh (1979) who found that, apart from the initial events in the male, post-embryonic gonadogenesis is reproducibly oriented with regard to the axes of the gonad rather than to those of the body.
Conservation and divergence of related neuronal lineages in the Drosophila central brain
Sulston, J. E, and Horvitz, H. R. (1981). Abnormal cell lineages in mutants of the nematode Caenorhabditis elegans.
The following cells were ablated in a series of animals: Da, Dp, Capa, Capp, Cppa, Cppp. In each case, the resultant larva lacked approximately the quota of muscles which the dead precursor would normally have made (accurate muscle counts, especially in damaged animals, are difficult). The missing cells left a gap, and the remaining muscles did not spread out much to fill it. The experiments are subject to the caveat given for the early ablations.
The assignment of sublineages is often a matter for subjective judgment, in that two sections of the lineage may be alike in some respects and discrepant in others. Thus, ABalpaaa and ABarapaa give rise to sublineages identical except for the fate of one cell, and it is reasonable to suppose that identical programmes are being used by the two precursors; the fate of the one anomalous cell may be determined either by position or by additional intrinsic factors. A more extreme example is provided by the pair ABalapap and ABalappp; in this case a dividing cell in one version of the sublineage is replaced by a cell death in the other, but there are still enough common features to suggest a shared programme.
All reviewers and the editor in particular were extremely impressed with the extent of the work, his thoroughness and the potentially immense source of information that might emerge from these data. The visualization of the data is also extremely impressive.
Schierenberg, E, and Cassada, R. (1982). Cell division patterns and cell diversification in the nematode Caenorhabditis elegans.
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All of the embryonic lineage was followed by direct observation. This method currently gives the best resolution in space and time, but has the disadvantage that the number of cells which can be followed in a single individual is limited by the short-term memory of the observer. Events were recorded by sketching the nuclei, using a colour code to indicate depth. A camera lucida was used at first, but the effective resolution was reduced by this accessory, and the additional illumination required tended to damage the specimen. The best aid proved to be a pair of gossamer cross hairs in one eyepiece, under which the nucleus of interest could be located with the help of a gliding stage. The light was blocked whenever the specimen was not being viewed.
The embryonic cell linage of C. elegans
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Laufer, J. S, and von Ehrenstein, G. (1981). Nematode development after removal of egg cytoplasm: Absence of localised unbound determinants.
The authors should do two things. First, they should calculate NBLAST scores, and statistically test their differences before making claims like "similar" or "identical". Second, when comparing two neuron types they should show in the figure a graph with dot plots of the all by all NBLAST pairwise comparisons of the two hemilineages to be compared, as well as a representative image of each, side by side, so this difference can be appreciated. Having to jump from main figures to supplementary figures with tens of images and find the ones that look similar is extremely hard.
WA editors' note: the positions of the descendants of Caaa and Cpaa are inadvertantly reversed in this fig (Loer C. et al, WBG 10(3)120). It is likely that the hypodermis is primarily responsible for the overall architecture of the animal, but the way in which it achieves this is largely unknown. One hint comes from ablation experiments in the head, which suggest that tension in the head hypodermis is necessary for elongation of the tail (see Cell Interaction Experiments). Certainly the cuticle is not involved in the shaping process, because the first sign of cuticle formation is at 600-650 min. At this time the seam cells acquire large Golgi bodies visible by Nomarski microscopy (cf Singh and Sulston, 1978), and cuticle can be seen at the mouth and in the rectum. The paired lateral alae characteristic of the L1 do not appear until just before hatching, and are apparently generated by circumferential contraction of the seam-specific cuticle (as is the case for dauer larva alae (Singh and Sulston, 1978)).
On each side of the animal there is a longitudinal row of specialised hypodermal cells, called seam cells (H0-H2, V1-V6, T); they remain separate from the rest of the hypodermis, and are responsible for making the lateral cuticular ridges known as alae (Singh and Sulston, 1978). All except HO are blast cells in the wild type, and even HO has been seen to divide in certain mutants (E. Hedgecock, personal communication).
Unlike AOTUv4A, the AOTUv4B hemilineage consists of multiple morphological groups of AOTU-related neurons arising largely in a sequential manner (Figure 10U). This is akin to the AOTUv3B hemilineage. The AOTUv4B and AOTUv3B hemilineages have similarities in spatial as well as temporal patterning of neuron morphology. First, both produce P-topology neurons, then many BU-targeting dot-to-dot neurons, followed by midline-crossing neurons (Figure 10M–T).
The muscles and structural cells of the pharynx have a precise threefold rotational axis of symmetry, whilst the nervous system of the pharynx is bilaterally symmetrical. Broadly speaking, two of the three identical sets of mechanical elements are generated by bilaterally symmetrical lineages, and the third set is assembled by piecemeal recruitment. The threefold symmetrical arrays of the arcade, hypl, hyp4, and parts of the valves are produced in a similar fashion. This plan of development contrasts with that found for the vas deferens (formed in the larval male), in which structures having a threefold rotational axis of symmetry are generated by three equivalent precursor cells which give rise to identical sublineages (Kimble and Hirsh, 1979; Kimble, 1981).
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Ablation of ABplpap (three animals) and ABprpap (three animals) also caused problems. Of these animals, only one of the former hatched, apparently because the dying precursor interferes with closure of the ventral cleft. However, before the embryos burst, it was possible to see that the excretory cell was made only when ABplpap was present. The one animal that hatched lacked both the excretory cell and the rectum, as predicted, and failed to grow.
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Figure 9C), reminiscent of versatile neuron topology. Successive changes in morphology further occur within groups. Notably, the proximal elaborations progressively extend from the AOTU to the SP in the first as well as the last group of AOTUv3B neurons (arrows in Figure 9A–C and G–H), contrasting the gradual confinement from the SP to the AOTU in the initial group of AOTUv1A neurons (magenta in Figure 1—source data 1B1-5). In summary, the AOTUv3B hemilineage displays progressive changes in progeny morphology at both intra- and inter-group levels.
Early divisions of the founder cells. None of the experiments so far described have shed much light on this intermediate period.
Embryonic cell lineages and segregation of developmental potential in Caenorhabditis elegans
We have also followed the origin of the founder cells and certain later lineages in the embryo of Panagrellus redivivus. This nematode is of interest because Sternberg and Horvitz (1981, 1982) have shown that its postembryonic lineage is quite similar to that of C. elegans, and that the newly hatched animal contains the same set of blast cells with one addition. We find that this extra blast cell, known as T3, has the embryonic ancestry Caappa; it is therefore homologous with the neuron PVR of C. elegans. On the basis of Nomarski microscopy, PVR is absent from P. redivivus (Sternberg, personal communication). P. redivivus proved to have the same endodermal lineage as T. aceti, to which it is closely related (Ritter, 1975); in one individual, however, division of Ea(1/r)ap resulted in an intestine having 20 cells instead of the usual 18.
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Another technique for killing individual cells is treatment with psoralen followed by irradiation with an ultraviolet microbeam. In this way James Priess (personal communication) has shown that removal of E or Ea precludes normal morphogenesis of the head, and that certain late divisions and deaths are dependent upon the presence of unrelated cells. The source and specificity of the implied inductive influences remain to be discovered.
In each series of PAM neurons, we identified 17 types of PAM neurons based on MB lobe innervation patterns (Figure 11A). This list covers all 14 previously reported types of PAM neurons plus three undocumented morphological types (r4 <r2, r4r5, and b’2r5). In addition, we observe variants of b2, r5, r4, and b’2 p that arise in separate windows and show birth time-dependent patterns of dendrite elaboration (Figure 11B).
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WA editors' note: In this paper, the positions of the descendants of Caaa and Cpaa are reversed in Figures 7a (260 min), 10 (290 min), 13 (L1) and 14 (L1). At 260 min, the four nuclei descended from Caaa are to be found on the left of the dorsal midline and those from Cpaa on the right.
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For H-class neurons with asymmetric neuropil targets, when their key asymmetric target is enclosed as extra information, we add ‘/’ in front of and italicize the enclosed neuropil name. We may add ‘i’ or ‘c’ after the neuropil name to indicate ‘ipsilateral’ or ‘contralateral’. Briefly, we have identified 467 morphological neuron types from 25 Vnd hemilineages in the fly central brain (Supplementary file 2). The five most heterogeneous hemilineages are: ALv1(A) (46 types), VLPa2(A) (37 types), LALv1B (31 types), LALv1A (29 types), and CREa1A (26 types). The five least heterogeneous are: FLAa1(B) (five types), FLAa3(A) (seven types), CREa1B (nine types), SLPpm3(B) (11 types), and VESa1(A) (12 types). The remaining 15 hemilineages yield 15 to 24 morphological neuron types. As a caveat, we could have over-estimated neuron types due to structural plasticity or we could have under-estimated neuron types due to lack of landmarks, particularly in neuropils that are not well-characterized.
The members of each pair are equivalent, but in certain cases they compete for a particular "primary" fate (Sulston and White, 1980). The presumptive G2/W and duct/G1 move to the ventral midline and compete for a primary fate in the same way but at an earlier time.
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Figure 20. Neurons of Dx class passing through basement membranes(arrowheads) and forming electrical junctions with muscle cells (mu). Electron micrograph of transverse section series 4. Bar = 1 µm.
As a result of this heterogeneity of ancestry with respect to cell fate, many lineal boundaries cross the various somatic structures in an apparently meaningless way. For example, the neurons and supporting cells of a given embryonic sensillum never arise as an exclusive clone, and the boundary between AB and MS meanders through binucleate cells.
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For reconstruction of the anterior sensilla, L4 larvae and adults were prepared as follows. The nematode was transferred to 3% glutaraldehyde in 0/1 M Hepes, pH 7/4, and immediately cut in the posterior half. After about 2 min a second cut was made in the anterior half; after 1 hr the head was washed three times with 0/1 M Hepes, pH 7/4, and then postfixed with 1% OsO4 in the same buffer for 1 hr. The specimen was embedded as usual (Ward et al, 1975), and about 200 serial sections were cut from the anterior tip.
Nevertheless, their initial divisions may be equational. In particular, the first anaphase of AB is transverse across the midline, and only at telophase do its daughters skew into an anterior-posterior configuration; this progression is seen more clearly in Ascaris, in which the transverse arrangement persists for much longer.
Chalfie, M, Horvitz, H. R, and Sulston, J. E. (1981). Mutations that lead to reiterations in the cell lineages of C. elegans.
However, you do not provide a molecular support for this for central brain neuroblasts, and it is quite surprising that nothing is known about the factors that might play a role in Type I neuroblasts. I admit that this is inferred from previous work from Chris Doe's lab (and Claude's lab as well) but it would be important to devise a way to access these potential factors. I am sure that you great creativity could allow you to develop an approach to test for genes expressed at different times in different neurons. I would not ask you to do this now as this would require much time, but you must discuss the issue of temporal patterning of Type I central brain neuroblasts.
Following the brief production of morphologically identical FB neuron types, both CREa1A and CREa2A NBs yield PAM neurons until they exit the cell cycle. Despite the serial production of different PAM neurons, the CREa1A and CREa2A PAM neurons (identified based on their paired sister neurons) look the same at all time points. This phenomenon indicates that the two NBs produce two identical series of PAM neurons.
The possibilities for regulation of cell shape seem to be rather limited. For this reason, ablation of a blastomere which generates a substantial patch (https://dkluchezar.ru/hack/?patch=2129) of hypodermis usually leads to a burst embryo. Individual muscles and Postembryonic blast cells lie in approximately their usual positions even when a number of their fellows have been lost.
Chalfie, M, and Sulston, J. (1981). Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans.
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Cell boundaries visible by Nomarski microscopy (because of surface depression) are shown as dotted lines. Numbers are to provide continuity and have no other significance. Cpapp(a/p) and Caapp(a/p) (see figure 7b) countermigrate similarly, but are only visible from the ventral side at this stage. WA editors' note: the positions of the descendants of Caaa and Cpaa are inadvertantly reversed in this fig (Loer C. et al, WBG 10(3)120).
Although these diagrams were prepared with the aid of a camera lucida they are not intended to show the absolute positions of cells, which in any case vary appreciably from one individual to another; what is reproducible is the neighbourhood of each cell at a given time. The patterns change rapidly, but the behaviour of each cell is characteristic and provides an additional check on its identity. An inexperienced observer should be able to identify nuclei in the diagrams unambiguously by starting one division earlier and checking the arrangement of sister cells.
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The latter observations suggest further that the precursors are determined, not by interaction with their neighbours, but by their ancestry. Evidence in favour of this conjecture was obtained from a series of laser ablation experiments, in which all tested precursors behaved autonomously. Some implications of this finding are discussed below (Symmetry and Asymmetry).
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The resulting larvae were scored, by Nomarski microscopy, for the postembryonic blast cells and certain neurons; although the blast cells were sometimes displaced in experimental animals they could still be accurately identified by their division patterns. With one exception (see below), the only blast cells missing were those normally generated by the ablated precursor. Furthermore, the surviving blast cells behaved normally during Postembryonic development, even to the extent of respecting the equivalence group boundaries (Sulston and White, 1980) in the usual way.
Despite stark differences between sister hemilineages, we see striking similarities between select hemilineages from different NBs. This phenomenon is evident when comparing the sister AOTUv4A and AOTUv4B hemilineages with the unrelated LALv1A and AOTUv3B hemilineages, respectively.
After 430 min the tip of the head elongates and the pharynx grows forward through the mass of neurons surrounding the developing nerve ring; at the same time the head becomes thinner. The pattern of neurons changes rapidly at first but stabilises after about 2 hr. In late embryogenesis it is possible to recognise all the neurons in the ring ganglion by their positions; at hatching the arrangement of the most posterior ones changes in an unpredictable way, perhaps as a result of pharyngeal movements.
The mingling in ancestry is most extensive in the pharynx. For example, there are three cases of neurons which are sisters to muscles (strictly, myo-epithelial cells), showing that divergence between these two fates can occur as late as the terminal division. Conversely, a consideration of symmetry and patterns of cell fusion in muscle rings m3, m4, and m5 (see Alimentary Tract and Appendix) indicates that a particular cell type may be generated by more than one developmental pathway.
Our current interest in the cell lineage of a particular nematode, Caenorhabditis elegans, has arisen as part of a larger research effort comprising genetic, anatomical, and biochemical approaches to the development of this animal. The lineage is of significance both for what it can tell us immediately about relationships between cells and also as a framework into which future observations can be fitted.
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There does exist recurrent relatedness at the sub-structural level in the AOTUv3 B hemilineage, as highlighted with arrows in Figure 9A-H and further validated by NBLAST analysis (Figure 1—figure supplement 2C). Because multiple features may recur at different frequencies, we could not confidently determine if the paired A/B hemilineages show coordinated or independent reoccurrences. We therefore did not to comment on patterns of recurrences across paired sister hemilineages.
Strome, S, and Wood, W. B. (1982). Immunofluorescence, visualization of germ-line-specific cytoplasmic granules in embryos, larvae, and adults of Caenorhabditis elegans.
Gossett, L. A, Hecht, R. M, and Epstein, H. F. (1982). Muscle differentiation in normal and cleavage-arrested mutant embryos of Caenorhabditis elegans.
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The three g1 gland cells migrate in a reproducible way. Their movements approximately follow the subsequent course of their secretory processes, and may be responsible for laying down the latter. The cell bodies of the anterior muscles and epidermis also move substantially in late embryogenesis (compare figure 8c with Albertson and Thomson (1976)).
The intestine is derived exclusively from founder cell E, which gives rise to no other tissue. The daughters of E are the first cells to enter the body cavity during gastrulation (90 min). By 300 min they have formed two rows of eight cells, one on the left and one on the right. The anterior pair divide dorso-ventrally to yield int1, which attaches to the pharyngo-intestinal valve.
Thank you for submitting your article "Conservation and divergence of related neuronal lineages in the Drosophila central brain" for consideration by eLife. Your article has been reviewed by two peer reviewers, and the evaluation has been overseen by Claude Desplan as the Reviewing Editor and K VijayRaghavan as the Senior Editor. The reviewers have opted to remain anonymous.
There are 12 additional (52% in total) Vnd hemilineages which, like LALv1B, contain multiple neuron groups targeting discrete sets of neuropils. This list includes four unpaired hemilineages (VESa1(A), VESa2(A), FLAa2(A), WEDd1(B)), five paired with a single-group hemilineage (LALv1B, CREa1B, CREa2B, AOTUv1A, AOTUv4B), and two pairs of sister hemilineages (SMPp&v1A/B, AOTUv3A/B). Among them, we see successive neuropil targeting only in four hemilineages and recurrent neuropil targeting (same pattern in multiple windows) in SMPp&v1A, SMPp&v1B, CREa2B, AOTUv3A, AOTUv4B, VESa1(A), VESa2(A), FLAa2(A), and WEDd1(B). Below, we utilize the paired AOTUv3B and AOTUv3A hemilineages to illustrate the successive versus recurrent targeting of discrete neuropils by serially derived neurons.
Sulston, J. E, Albertson, D. G, and Thomson, J. N. (1980). The Caenorhabditis elegans male: Postembryonic development of non-gonadal structures.
However, we do not know exactly how the opposite Imp/Syp protein gradients can define ~30 serial temporal fates in a protracted neuronal lineage. Interestingly, recurrent production of related neuron types has emerged as a dominant theme in the temporal patterning of Vnd lineages. Dynamic Notch signaling may underlie some alternating temporal fates, as Notch has been shown to control alternate production of AL and AMMC projection neurons in the lateral AL lineage (Lin et al, 2021). However, it is unlikely that Notch alone can mediate multiple recurring features as seen in most Vnd hemilineages. We therefore propose involvement of parallel recurring factors to elicit unsynchronized repetition of distinct features. In sum, there likely exist multiple temporal fating mechanisms that act in concert to expand neuron diversity, thus resulting in complex temporal patterns (Figure 14C).
For pairwise comparison of Vnd neuron types by NBLAST, we selected 464 segmented neurons that were warped into a standard adult fly brain template. We then generated the all-to-all score matrix using the NBLAST package available at GitHub (https://github.com/jefferislab/NBLAST_on-the-fly). Various analyses of the score matrix and visualization of the results were carried out by Python.
By contrast, we see the recurrence of neurons with characteristic morphology in the AOTUv3A hemilineage (Figure 9I–P). All AOTUv3A neurons project across the brain midline through the same commissure.
Starting from the anterior part of the egg, the cells spread over the entire surface except for the posterior dorsal region. Some of them lie inside the head temporarily at an early stage. Towards the end of gastrulation the AB pharyngeal precursors enter the interior through the ventral side of the head, and, later still, four muscles and the rectal cells sink into the ventral surface of the tail.
The hypodermis is a sheet of cells which forms the outer surface of the nematode and secretes the cuticle. Its postembryonic development has been described by Sulston and Horvitz (1977), and other aspects have been discussed by White (1974) and by Singh and Sulston (1978), but no comprehensive account has previously been given.
Ablation of P4 led to the production of larvae with no germ line. The somatic gonads of these animals grow more or less normally but are devoid of gametes: P4 is not replaced by any other cell.
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The alimentary tract is a single tube which comprises the following components: (mouth), buccal cavity, pharynx, pharyngo-intestinal valve, intestine, intestino-rectal valve, rectum, (anus). Part of it is shown schematically in figure 17.
The exception was that, after the ablation of ABplapa, W was missing and G2 was present. In these animals ABprapaapa, which normally becomes W, presumably became G2 in place of the missing ABplapaapa. This example of regulative interaction was confirmed by the direct ablation of ABplapaapa (one animal) and ABprapaapa (two animals) at 260 min, before the cells moved ventrally: all three animals subsequently formed G2 and lacked W.
Ablation is more difficult in eggs than in larvae. Small cells can be killed satisfactorily (although it is difficult to avoid damage to their neighbours), but attempts to kill the large cells present early in embryogenesis frequently cause death of the entire embryo. Damage to these young eggs can be minimised by mounting them on 1% agar in an isotonic medium (see Light Microscopy: T. aceti), since heavy pulses seem sometimes to cause the shell to leak transiently. In this way the nucleus of any given cell can be destroyed, or at least prevented from dividing; although the cytoplasm inevitably persists, it is often displaced from its usual position. The technique used is to pulse the target cell repeatedly at an energy level sufficient to produce refractile debris in its nucleus; whenever the cell appears dangerously weakened (low refractility of the cytoplasm, excessive Brownian motion) it is rested for a minute or two before pulsing is continued. After a successful operation the cell, heavily loaded with refractile debris, appears largely to have lost contact with its neighbours and remains visible as an undivided blob.
Body cavity is termed a pseudocoelom, since intestine is in direct contact with body wall. Principal changes during postembryonic development are: overall increase in size; growth and maturation of the gonad; formation of vulva (midventral) in hermaphrodite, and copulatory bursa (posterior) in male, both with associated musculature; cell division in hypodermis and ventral nervous system. Sensilla generated postembryonically are: postdeirids (paired, lateral, between gonad and anus) and ventral microtubule neurons in both sexes; numerous sensilla in the male copulatory bursa (Sulston et al, 1980).
Related lineages make similar neurons in comparable temporal patterns
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The cells which were not identifiable at this stage (mainly interneurons and motorneurons) were followed in small groups until the animal hatched. These observations are tedious because from 450 min onwards the embryo rotates continually about its longitudinal axis, and it is necessary to train the eye to rapid pattern recognition for each cell group in turn. After hatching, some cells were identified from previously known L1 anatomy (J. G. White et al, unpublished) and the remainder were traced into the adult. This is a relatively easy task because the larvae do not rotate and the patterns change only slowly, so that an entire ganglion can be followed in one individual.
In addition to bilateral symmetry (see Sublineages) parts of the nematode display two, three, four, and sixfold rotational axes of symmetry. The embryonic lineage, on the other hand, is in part bilaterally symmetrical and in part asymmetrical; the ways in which it generates the more elaborate symmetries of the mature nematode will now be discussed.
Given that hemilineages are distinct, our following analyses of neuron diversity independently considered the 25 hemilineages. Nonetheless, in the seven lineages composed of sister hemilineages, we exploited the paired sister-neurons to compare sister-hemilineage development.
The developers decided to unite the players among themselves, taking into account the innovations that they thought over and introduced. For example, they made it much easier to get to level 75 and above. A significant step was also made to improve communication between players since the reward for killing monsters during a group passage of a location was significantly increased. This served as a confirmation of the collective nature of the passage of the game. The benefit of killing other characters has also been significantly reduced. Although the drop of things has become a more common fact, the amount of experience gained for this has significantly decreased. This is how the system of protection against aggressive charms was implemented.
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The tail is completed by three mononucleate cells (hyp8, 9, 11) and a binucleate cell (hyp10). All the hypodermal syncytia arise as mononucleate cells which subsequently fuse together.
This section describes some investigations using the technique of cell ablation by means of a laser micro-beam (Sulston and White, 1980). Although the number of experimental animals is small, the invariance of the wild-type lineages ensures that any abnormalities observed are highly significant.
Wright, K. A, and Thomson, J. N. (1981). The buccal capsule of Caenorhabditis elegans (Nematoda: Rhabditoidea): An ultrastructural study.