Lucernaria, O. F. Muller, 1776
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publication ID |
https://doi.org/ 10.1007/s13127-020-00459-8 |
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persistent identifier |
https://treatment.plazi.org/id/821B879C-713D-FFF0-FF0F-5E9BC454FEBC |
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treatment provided by |
Felipe |
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scientific name |
Lucernaria |
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Planula of Lucernaria View in CoL : “ hairless worm ” in an otherwise ciliated world of cnidarians?
The endoderm cells differ from the ectoderm cells by the high content of small and medium sized vacuoles; this difference becomes already visible in the beginning of AP axis differentiation ( Fig. 5c, d View Fig ). When a planula hatches, the vacuoles in the endoderm cells increase their size ( Fig. 8c View Fig ) probably by fusing with one another. Then, when the larva spends a while in seawater, the vacuoles expand dramatically (Fig. 9h, i, purple arrows) increasing the length of the endoderm rod and, therefore, the whole planula body ( Fig. 10n, o View Fig ). Most likely, the rod elongates by the same mechanism as the notochord of amphibians and fish, where vacuoles swell osmotically ( Adams et al. 1990; Thomas and Stemple 2004). Swelling of endoderm cell is a mechanism, by which hatched larvae not only increase their length, but also obtain hydrostatic skeleton probably contributing to their movement.
Staurozoan planula crawls on the substrate making vermiform moves ( Kowalevsky 1884; Otto 1976) provided by contractions of longitudinal and circumferential processes of myoepithelial cells (Fig. 9d). Since cells and body are comparable in size due to low cell number, all changes in planula body shape (bending, stretching, etc.) induce deformation of individual cells, both ectoderm and endoderm (Fig. 9e, f).
Since the time of first discovery of weird looking staurozoan larvae, it has been considered that these planulae lack cilia, and that is why they crawl instead of swim ( Hanaoka 1934; Kowalevsky 1884; Otto 1976). However, we revealed a very short cilium on each ectoderm cell ( Figs. 8b View Fig , 9n–n″, 9o, o′). These cilia are reminiscent of rudimentary cilia, emerging either transiently during cell differentiation ( Boelsterli 1977) or remaining as a rudiment in differentiated cells ( Gardiner and Rieger 1980; Rieger and Lombardi 1987). Obviously, they cannot function as a propelling tool, since they even do not have an upright position and their number is ridiculously small; nevertheless, we cannot exclude that they do have certain role in planula life.
Staurozoan larvae were known to develop cnidocytes at the posterior third of the body in a few days after hatching ( Kowalevsky 1884; Wietrzykowski 1912). Our ultrastructural analysis reveals that differentiation of capsules begins earlier, right after hatching ( Fig. 8a, d, e View Fig ). Moreover, we assume that the commitment of these cells to cnidocyte pathway occurs much earlier, at the beginning of AP axis differentiation: it is likely, that rounded basiepithelial cells ( Figs. 5 View Fig , 6 View Fig , 7, 10) are in fact cnidoblasts at an early stage of differentiation. Though they do not have morphological characteristics (capsule, thread) of a cnidoblast, their shape, size, and location are very similar to those of cnidoblasts of planulae.
Evolutionary trend towards a reduction in number of cells in early development: bypassing constraints
Our study showed that early development of Lucernaria is very similar to that of other staurozoans ( Lucernaria campanulate (= Calvadosia campanulata ), Halyclistus steBnegeri, Halyclistus salpinx, Halyclistus octoradius, and Thaumatoscyphus distinctus (= Manania uchidai )) ( Bergh 1888; Hanaoka 1934; Kowalevsky 1884; Miranda et al. 2018; Otto 1976; Wietrzykowski 1910, 1912). So, it is implausible that these ontogenies evolved independently. Since these species belong to both suborders of Staurozoa, Myostaurida and Amyostaurida ( Miranda et al. 2016, 2018), we hypothesize that the trend towards the reduction of cell number in early development emerged very early in staurozoan evolution.
It is important to note that embryos of many other cnidarian species consist of much higher number of cells than the staurozoan ones. In the hydrozoan Hydractinia , gastrulation by delamination starts at the 32-cell stage, but mid-gastrula stage embryos already consist of about 2000 cells ( Kraus et al. 2014; Plickert et al. 1988). The hydrozoan Clytia gastrulates by unipolar ingression, and embryos have approximately 800 cells in the very beginning of gastrulation (according to images from Kraus et al. 2020). The similar number of cells (700–1000) were found in early gastrula stage embryos of the scyphozoan Aurelia ( Yuan et al. 2008) . What exact constraints do the embryos evolving towards low cell number face? A depleted set of morphogenetic processes as we have seen in Lucernaria ( Fig. 12a–e View Fig ). If we analyze the set of morphogenetic movements available for medusozoan cnidarians ( Hydrozoa, Scyphozoa, and Staurozoa) ( Fig. 12 View Fig ), we find that some developmental trajectories are not accessible for staurozoans by default, as they are based on the coherent behavior of multiple cells. These trajectories are based on invagination ( Fig. 12a, h, j, k View Fig ), which is characteristic for scyphozoans, and on the ingression of multiple cells ( Fig. 12a, h, i, k View Fig ), which is very typical for hydrozoans ( Berrill 1949; Byrum 2001; Kraus et al. 2020; Metschnikoff 1886). Some other trajectories, e.g., primary and secondary delamination ( Fig. 12a, f, g, k and a, h, g, k View Fig ), occurring in hydrozoan embryos ( Kraus and Markov 2017; van de Vyver 1964), were not realized in staurozoan evolution. If we assume that the staurozoan’ s common ancestor gastrulated by invagination, then the reason for this absence is, perhaps, evolutionary history of the group (so-called phylogenetic inertia) since ingression, unlike delamination, is easily derived from invagination ( van der Sande et al. 2020). We can only speculate that transitions to high number of cells during cleavage ( Fig. 12h View Fig ) or gastrula stages ( Fig. 12g View Fig ) are constrained by the natural selection favoring the reduction of cell number in staurozoan embryos.
Staurozoans are not unique in having few cells in embryos. There is a wide range of groups such as Nematoda, Rotifera, Gastrotricha, Sipunculida, Gastropoda, and Tunicata, some representatives of which have small number of cells in their embryos. Nonetheless, they all end up developing phylumspecific bauplans ( Hejnol 2010; Schierenberg 2001; Schulze and Schierenberg 2011). This means that these animals successfully bypass the constraints imposed by the number of cells using very peculiar developmental trajectories.
What is so peculiar in developmental trajectories of the animals having very few cells in embryos? Remarkably, early embryos of Lucernaria and the aforementioned animals from very distant phylogenetic groups look very similar. Their blastula lacks (or almost lacks) blastocoel and consists of 16–64 blastomeres, blastomeres are large in relation to the size of an embryo, vegetal cells are often (but not always!) bigger than animal ones. It is not surprising that morphogenetic movements during gastrulation in these animals look the same: presumptive endoderm, which consists of very few cells (e.g., only 2 cells in nematodes and gastrotrichs) undergoes very peculiar type of ingression that was called “dense ingression” ( Ivanova-Kazas 1995). During dense ingression, presumptive endoderm cells do not ingress and crawl inside the embryo one by one to fill the blastocoel. Instead, they redistribute cell contents and detach apices, and this is enough to bring these cells to their final position. Dense ingression is always followed by epiboly of ectoderm cells ( Ivanova-Kazas 1995).
Indeed, the mode of gastrulation strongly depends on the number of cells. The tunicate appendicularians have 32-cell blastula and gastrulate by ingression followed by epiboly ( Fujii et al. 2008). However, 76–110 cells seem to be enough for the embryos to gastrulate by invagination that is observed in other tunicates, specifically ascidians ( Jeffery 1992; Nishida 1986). Likewise, the low cell number embryos of nematodes gastrulate by ingression ( Schierenberg 2006; Sulston et al. 1983), while nematodes with higher number of cells gastrulate by invagination ( Schulze and Schierenberg 2011).
Therefore, in the embryos with low number of cells, cell reshaping substitutes actual cell movements. This we observe not only in gastrulation but also in the process of cell intercalation occurring during endoderm rod formation in Lucernaria or during dorsal epidermal intercalation in C. elegans ( Chin-Sang and Chisholm 2000) . It seems that epithelial sheet morphogeneses (such as epithelial folding) are rarely employed in the development of low cell number embryos. For instance, appendicularian neurulation does not rely on the folding of neural plate ( Fujii et al. 2008).
Another constraint, which could affect the development of animals evolving towards the reduction of cell number in embryos and larvae, is a low threshold of mechanical instability that could decrease developmental robustness. In the embryos with high number of cells (such as amphibians), changes in the shape and mechanical state of individual cells add up to mechanical state and reshaping of tissues only if they occur in multiple cells at once. As we described for Lucernaria , each individual cell constitutes so large a part of an embryo or larva, that reshaping of any cell immediately leads to changes in the mechanical state of the whole organism and may trigger dramatic developmental consequences. We can find very similar situation in ascidians, where the blastopore lip consists (on sections) of only one cell, which does almost the same job as the multicellular blastopore lip in vertebrate embryos ( Sherrard et al. 2010).
Therefore, low cell number embryos “had to learn” how to provide developmental robustness under an increased morphogenetic role of each individual embryonic cell.
It was inferred that in few cell embryos of Nematoda, Spiralia, and Chordata developmental trajectories include, but are not limited to, determinant rather than regulative developmental mode; early establishment of cell linages; high importance of maternal transcriptional factors; fast life cycle ( Hejnol 2010; Holland 2014; Lambert 2010; Schulze and Schierenberg 2011). A reduced role of regulative genes in early development is reflected in that the genes are clustered in operons in both nematodes and ascidians ( Blumenthal et al. 2005; Denoeud et al. 2010; Paps et al. 2012; Pettitt et al. 2014; Satou et al. 2008; Tsagkogeorga et al. 2012). Moreover, many Hox genes were lost in nematodes ( Aboobaker and Blaxter 2010) and tunicates ( Ikuta and Saiga 2005; Seo et al. 2004). It will be interesting to find out if staurozoans follow these trends and to what extent, especially taking into account that early establishment of cell linages and mosaic development are not typical for cnidarians in general.
The much more challenging question is why the animals would reprogram their development for reduction of cell number in embryos. One possible explanation is that this might be the way to accelerate early development: the embryo does not waste time and energy on multiple cell divisions and starts gastrulating when it contains just a few dozen cells. By acceleration of early development animals might benefit from the temporal reduction of the stage of vulnerable, defenseless, and non-feeding embryo ( Strathmann et al. 2002) or from favorable conditions in ecologically unstable biotopes ( Schierenberg 2001). On the other hand, reduction of cell number can be considered as a side-effect of a positive selection for the higher fecundity, that is typical for sedentary animals or animals facing unstable environment. Production of minute size eggs enables the increased number of offspring ( Carrière and Roff 1995; Rosenheim 1996). Since there are certain limits in cell size diminution ( Polilov 2015, 2016), the decrease of embryo size from a certain point could be reached by decrease of blastomere number only, not blastomere size. However, reduction of cell number does not always correlate with small size of an egg. For example, in spiralians, low number of cells at the gastrula stage is a characteristic feature of species with relatively big yolky eggs ( Hejnol 2010; Ivanova-Kazas 1995).
We can only speculate on the scenario of Lucernaria ontogeny evolution, but there is an obvious causal connection between evolutionary changes in the number of embryonic cells and in the life cycle and reproductive strategy.
Taken together, we described and analyzed the dynamics of cell shape changes during early development of the staurozoan Lucernaria . From our data, we inferred how the embryo overcomes the constraints imposed by the low number of cells by using very peculiar developmental trajectory. We reconstructed the morphogenetic bases of this trajectory and suggested a link between morphogenetic movements and mechanical stresses orchestrating the development of a few cell embryo. This is the first step in our understanding of the development of these fascinating animals; the next steps will require unraveling molecular basis of morphogenetic events described here. Moreover, little is known about metamorphosis in staurozoans: there are no convincing data on the morphogenesis of a primary polyp, which is another mystery of this unique group.
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