The Nereid on the rise: Platynereis as a model system

The Nereid Platynereis dumerilii (Audouin and Milne Edwards (Annales des Sciences Naturelles 1:195–269, 1833) is a marine annelid that belongs to the Nereididae, a family of errant polychaete worms. The Nereid shows a pelago-benthic life cycle: as a general characteristic for the superphylum of Lophotrochozoa/Spiralia, it has spirally cleaving embryos developing into swimming trochophore larvae. The larvae then metamorphose into benthic worms living in self-spun tubes on macroalgae. Platynereis is used as a model for genetics, regeneration, reproduction biology, development, evolution, chronobiology, neurobiology, ecology, ecotoxicology, and most recently also for connectomics and single-cell genomics. Research on the Nereid started with studies on eye development and spiralian embryogenesis in the nineteenth and early twentieth centuries. Transitioning into the molecular era, Platynereis research focused on posterior growth and regeneration, neuroendocrinology, circadian and lunar cycles, fertilization, and oocyte maturation. Other work covered segmentation, photoreceptors and other sensory cells, nephridia, and population dynamics. Most recently, the unique advantages of the Nereid young worm for whole-body volume electron microscopy and single-cell sequencing became apparent, enabling the tracing of all neurons in its rope-ladder-like central nervous system, and the construction of multimodal cellular atlases. Here, we provide an overview of current topics and methodologies for P. dumerilii, with the aim of stimulating further interest into our unique model and expanding the active and vibrant Platynereis community.

The Development and Setting of a Serpulid Worm, Hydroides norvegica Gunnerus (Polychaeta)

Hydroides norvegica larvae were reared to settling in 8-10 days at 20°C. The paired conical processes on the collar setae characteristic of the genera Hydroides and Serpula were developed in the larvae by the sixth day. Settling differed from that recorded for other larvae in that (i) larvae could become attached to surfaces comparatively early in their free-swimming life, (ii) "searching" behaviour followed by settling on a particular locus was not observed, (iii) feeding continued through metamorphosis. The primary operculum of the young worm was formed by modification of the third branchial filament of the left side. Certain identification as H. norvegica could not be made until this had been shed and replaced by a secondary operculum developed from the right side 4-8 weeks after metamorphosis.

Memoirs: The Development of the Sabellid Branchiomma vesiculosum

1. Larvae of Branchiomma vesiculosum Montagu were obtained from artificial fertilizations, and reared through metamorphosis and for some weeks afterwards. 2. The larvae are extremely yolky and do not feed until after metamorphosis. They swim by means of a broad prototroch, and are provided with a pair of cup-shaped eye-spots, a large head vesicle, and two anal vesicles. There is a broad neurotroch but no telotroch. The mouth is open but the anus is closed. In the last swimming stages rudiments of the adult branchial apparatus appear as a pair of lobed swellings, behind the eyes but in front of the prototroch. Behind the latter the collar rudiments appear. There are usually three or four chaetigerous segments marked out when metamorphosis sets in. 3. The metamorphosing larva settles on the bottom, and secretes for itself a tube of mucus. The prototroch and larval tissues (episphere) of the head clump together to form a large snout-like structure. This gradually breaks up into small pieces which are thrown off one by one as they are formed. With the loss of the prototroch and other larval head tissues the adult part of the head becomes joined on to the trunk. At the same time the branchial rudiments branch to form pinnules, which are directed forwards so that their bases overlap the eyes. The anus opens, and the young worm begins to feed. Metamorphosis occupies about four days. 4. The larval stages and the metamorphosis have been studied in histological, and to a limited extent in cytological, detail. Apart from the curious metamorphosis, which to some extent recalls that of Owenia and Polygordius, the development shows no striking features. 5. After metamorphosis the worm elongates by the addition of setigers in front of the pygidium. These are at first of the thoracic type (dorsal bristles, ventral uncini), but when the ninth and succeeding setigers appear they show abdominal constitution (dorsal uncini, ventral bristles) from the first. Thus no setigers change over from abdominal to thoracic constitution as they do in the development of young Serpulid worms. 6. Coincident with the loss of the neurotroch at metamorphosis the mid-dorsal line of the head and trunk of the young worm becomes ciliated to form the faecal groove of the adult. This strip of cilia continues on the ventral surfaces of the ninth and succeeding setigers, after passing round the right side between the eighth and ninth bristle segments. For a time the intersegmental groove between these segments is ciliated on the left side as well. 7. The branchial rudiments, which began to branch before metamorphosis, continue steadily to branch and grow afterwards. The pinnules are supported by an internal skeleton of thick-walled cells to the base of which the main dorsal and ventral longitudinal muscles of the body become attached. The most dorsal branch of each branchial rudiment, lying close to the mid-dorsal line, forms one of the so-called palps of the adult and is not supported by an internal skeleton. 8. The manner in which the young worms build their first sandy tube is described. 9. Early larvae of Sabella pavonina (Savigny) are described. They closely resemble those of Branchiomma. 10. The present position of embryological knowledge concerning the Polychaetes is very briefly summarized. It is shown that Sabellid larvae are more closely related to Serpulids than to those of any other family.

The Development of Audouinia tentaculata (Montagu)

(1) Adults of Audouinia tentaculata Montagu were induced to spawn in the laboratory; the eggs were fertilized and the larvæ reared to metamorphosis and early bottom stages for the first time.(2) The larvæ are yolky and do not feed. They have a broad prototroch and telotroch and a broad neurotroch. The ciliation of the head is rather complex. There are no bristles. When about ten days old they metamorphose.(3) During metamorphosis most of the cilia, except those of the neurotroch, disappear and their cells are absorbed internally.(4) Bristles appear for the first time a few days after metamorphosis. After a while branchiæ appear, followed by what are apparently tentacular filaments situated on segments anterior to those on which they occur in the adult.(5) Discussion centres on the position of the tentacular filaments and the first pair of branchial filaments in the young worm as compared with the adult. The segmentation of the anterior achaetigerous region also receives attention.

Development of Scolecolepis fuliginosa (Claparède)

1. The development of Scolecolepis fuliginosa (Claparède) is described from the egg to the young worm for the first time.2. Comparison of reared larvæ with larvse from the plankton did not reveal any important difference.3. The eggs are pelagic, and are similar to those of Nerine.4. A description is given of the histological structure of a ciliated pit which arises in early larval existence and disappears at metamorphosis. The structure of the glandular region of the pygidium is also described.5. It is apparent that from the attainment of the fourth setiger onwards, the centre of differentiation is located in the third setiger, so that segmental structures arise first in this segment and then appear in the first and second setigers as well as in the succeeding ones.6. The larva of Scolecolepis has three pairs of eyes, the third pair disappearing in the young worm long after metamorphosis is otherwise complete.

The Larvæ of the British Sabellarians

SUMMARY1. Sabellaria alveolata Linnæus has been reared for the first time from the egg through the pelagic stages and metamorphosis to early bottom stages. The chief features in the development of the external characters are described and special attention is drawn to the existence of peculiar grasping-cilia on the telotroch. The manner in which the young worm builds its first tube of sand grains is also described.2. Sabellaria spinulosa Leuckart has similarly been reared for the first time from the egg to early bottom stages. Its development is very similar to that of the preceding species, but during the later pelagic life the two can easily be separated, as the primary palese of the crown, which appear among the long provisional bristles of the first pair of parapodia, show a marked specific difference. The early stages cannot be distinguished.3. A larva which is probably that of the rare Pallasia murata Allen is described.4. A tentative key to the British Sabellarian Larvaæ is drawn up.5. The observations of previous workers are discussed. It is shown that Sabellarian larvaæ have frequently been described as the larvaæ of Spio or of Polydora, in spite of the fact that the early stages of Sabellaria had been obtained more than once from artificial fertilisations. Caullery was the first to point out the error, and he is fully confirmed in this paper.6. It is shown that the caudal appendage of a full-grown Sabellaria alveolata possesses internally a series of fifty or sixty transverse septa.

A Contribution to the Life History of Echinostomum secundum, Nicoll

In some notes on the Trematodes of Northumbria published in 1905 a few remarks were made on a larval Trematode inhabiting the liver of the common periwinkle Littorina littorea. The liver in two per cent. of the periwinkles from Budle Bay was full of rediæ containing cercariæ more or less developed, the latter agreeing in every way with an encysted Echinostomum larva which inhabits mussels, cockles and other bivalve mollusks in the same locality. So close was the resemblance that I had no hesitation in declaring them to be the same worm in different stages, but hoped for an opportunity of demonstrating this by experiment. In October 1908 through the courtesy of Professor Meek I had the opportunity of conducting some feeding experiments in the Dove Marine Laboratory, Cullercoats, which have given satisfactory results, and although it is not possible to state absolutely that the forms are identical yet the evidence is so strong that I think I am justified in regarding the young worm in the periwinkle as an earlier larval form of the encysted worm in the foot of the mussel and cockle.

Memoirs: On the Structure of an Earthworm allied to Nemertodrilus, Mich., with Observations on the Post-embryonic Development of Certain Organs

The principal new facts in this paper may be briefly summarised as follows : (1) The nephridial system consists of paired nephridia which do not open immediately on to the exterior, but are connected with an extensively ramifying system of tubes embedded in the circular and longitudinal muscular coats; these tubes consist of four principal longitudinal trunks continuous from segment to segment, and of a single large circular vessel in each segment passing right round the worm at the junction of the circular and longitudinal muscles; these are connected by a plexus of vessels, and numerous tubules, leading to the exterior, are given off from the circular trunk. In some of the genital segments the paired nephridia have almost disappeared, leaving only the integumental network. Nothing of the kind has been yet described in any Oligochæte. In the young worm, just escaped from the cocoon, there is no integumental network, which must, therefore, be regarded as secondary, but the anterior nephridia at any rate are connected on each side by a continuous longitudinal duct lying within the cœlom. (2) In the young worm the reproductive organs agree with these organs in other earthworms; in the^ adult, a large unpaired sac lying over the gut is developed; this sac encloses the receptacula ovorum, and opens by a median pore on Segment 13. It is developed from mesoblastic tissues, and is not therefore the morphological equivalent of the spermathecæ in Lumbricus, &c., but it performs the same function; the sac is formed internally and then grows out towards the epidermis ; it is at first in open communication with the cœlom; its front wall is formed out of the intersegmental septum between Segments 12, 13; the ovaries are enclosed by it, but disappear early, before the sac is completed; otherwise the ova would be probably unable to enter the egg-sac which becomes nearly completely shut off from the sac; the two are in communication only by the oviducal funnel, which has become divided by the growth of the spermathecal sac into two separate tubes, one opening into the spermathecal sac, the other into the closed egg-sac; they unite, of course, to form the oviduct itself, which opens on to the 15th segment, reckoning by the external furrow, but on to the border line between Segments 14, 15, reckoning by the septa. (3) The testes and the vas deferens funnels are quite typical in their structure and position; so, too, are the (two) pairs of sperm-sacs (in Segments 11, 12). The sperm ducts are not, as they are in other Eudrilidæ, dilated to form sperm reservoirs ; they open into tubular atria, with thick muscular walls and glandular lining, near to their blind extremities; the two atria open by a common pore upon the border line between Segments 17, 18; each is furnished with a short penial seta not ornamented. (4) The alimentary tract has no calciferous glands or ventral œsophageal pouches such as are found in other Eudrilidæ at the end of the oesophagus are three gizzards, one to a segment; the intestine which immediately follows has at first three typhlosolar folds; later on the two lateral and shorter folds disappear. The ventral wall of the pharynx is connected with the nephridial tubes of its segments; they open into the interior of the pharynx. (5) The area surrounding the setas of each side of the body is shut off from the general body-cavity, forming a paired series of chambers; in the œsophageal region is developed a perihæmal cœlomic space surrounding the subœsophageal vessels.