Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
, 18 (1), 149

Developmental Studies Provide New Insights Into the Evolution of Sense Organs in Sabellariidae (Annelida)

Affiliations

Developmental Studies Provide New Insights Into the Evolution of Sense Organs in Sabellariidae (Annelida)

Conrad Helm et al. BMC Evol Biol.

Abstract

Background: Sabellarids, also known as honeycomb or sandcastle worms, when building their tubes, produce chemical signals (free fatty acids) that are responsible for larval settlement and the formation of three-dimensional aggregations. The larval palps and the dorsal hump (becoming the median organ in adults) are presumed to participate in such a substrate selection during settlement. Notably, the sabellariid median organ is an apparently unique organ among annelids that has been attributed with a sensory function and perhaps with some affinities to the nuchal organs of other polychaetes. Nevertheless, detailed investigations of this prominent character complex including ultrastructural examinations are lacking so far.

Results: Our comprehensive investigations provide data about the anterior sensory organs in Sabellariidae and inform about their transformation during pelagic larval development. We used a comparative approach including immunostaining with subsequent confocal laser scanning microscopy (clsm), histological sections as well as electron microscopy in a range of larval and adult stages of two sabellariid species. We find that the neuronal innervation as well as the ultrastructure of the sabellariid ciliary structures along the median organ are highly comparable with that of nuchal organs known from other polychaetes. Furthermore, the myoinhibitory protein (MIP) - a protein known to be also involved into chemo-sensation - was detected in the region of the larval median organ. Moreover, we reveal the presence of an unusual type of photoreceptor as part of the median organ in Idanthyrsus australiensis with a corrugated sensory membrane ultrastructure unlike those observed in the segmental ocelli of other polychaetes.

Conclusions: We are describing for the first time the nuchal organ-like structures in different developmental stages of two species of Sabellariidae. The external morphology, neuronal innervation, developmental fate and ultrastructure of the newly-discovered median organ-based ciliary pits are comparable with the characteristics known for annelid nuchal organs and therefore indicate a homology of both sensory complexes. The presence of myoinhibitory peptide (MIP) in the respective region supports such a hypothesis and exhibits the possibility of an involvement of the entire sabellariid median organ complex, and in particular the prominent ciliated pits, in chemo-sensation.

Keywords: Larva; Median organ; Polychaetes; Sedentaria; Sensory organs; Settlement.

Conflict of interest statement

Ethics approval and consent to participate

No permits or authorizations were required to collect specimens of Sabellaria alveolata used in the study. The material of Idanthyrsus australiensis were collected from Long Reef, a marine reserve with a permit issued to the Australian Museum by NSW DPI (F86/2163–72 & OUT 13/2588).

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Schematic overview showing a nuchal organ of Nerillidium troglochaetoides (Nerillidae) illustrating the general organiszation of an annelid nuchal organ. The organ consists of ciliated supporting cells (sc) with microvilli and cilia (ci), an olfactory chamber (oc), and prominent sensory cells (sc) running towards the olfactory chamber (oc). The entire structure is embedded in the epidermis (ep) and can be retracted via a distinct retractor muscle (rm). cc, ciliated supporting cell; ci, cilium; cu, cuticle; ecm, extracellular matrix; ep, epidermis; oc, olfactory chamber; rm., retractor muscle; sc, sensory cells. The image was redrawn and modified from Purschke 1997 [20]
Fig. 2
Fig. 2
Scanning electron microscopic images of developmental stages of Sabellaria alveolata (a-d, g) and Idanthyrsus australiensis (e, f). Age of the larvae is given in days post fertilization (dpf) and the species identity is specified in the respective figure. In (a-c) anterior is left, in (e-f) anterior is up. d is a frontal view with the dorsal side up. a and b show a view from lateral. The inset in (b) shows a dorsal view with the anterior side up. c and (e-g) are dorsal views. The position of the larval median organ is marked by the white arrow and the position of the prominent ciliated tufts on the median organ is indicated by red dashed circles. a In pre-metamorphic larvae the prototroch (pt), telotroch (tt), the chaetae (ch) and the palps (pl) are well developed. The larval median organ is situated within the dorsal gap of the prototroch (pt), between the bases of the palps (pl). b A closer view reveals prominent ciliated tufts (red dashed ovals) and few additional cilia covering the surface of the larval median organ. The inset shows the same region in earlier larvae (~ 25 dpf) with palp (pl) buds already developing. Note the onset of the ciliation along the median organ. c A dorsal view reveals the position of the ciliated tufts at the base of the median organ. d In post-metamorphic specimens, the entire complex of the median organ is shifted from a dorsal towards a frontal position. The entire structure becomes flattened and incorporated in the formation of the juvenile anterior end. Nevertheless, the ciliated tufts (red dashed circles) are still detectable. e 26 dpf larvae of I. australiensis exhibit a median organ with a densely ciliated base. f The median organ is still well-developed even in larvae prior to metamorphosis. g In juveniles of S. alveolata the larval median organ is reduced in size, but still present as part of the anterior juvenile end. ch, chaetae; nh, nuchal hooks; op, opercular papillae; pa, palae; pl, palps; pt., prototroch; tt, telotroch. Scale bars: 20 μm (a-e), 10 μm (f) and 100 μm (g)
Fig. 3
Fig. 3
Development of the neuronal innervation (α-tub-LIR) of the larval median organ in S. alveolata (a) and I. australiensis (b-d). Confocal maximum projections. Anterior is up in all images. All views are dorsal, except of (d) which shows a view from apical. The position of the distinct ciliated tufts of the median organ is indicated by dashed circles and prominent perikarya at the tip of the median organ are marked with arrowheads. Age of the larvae is given in days post fertilization (dpf) and the species identity is specified in the respective figure. a The prominent prototroch (pt) as well as the innervating prototroch nerve (pn) are present in pre-metamorphic larvae of S. alveolata. The larval brain (br) consists of a ventral (vr) and dorsal root (dr) of the circumesophageal connective. Prominent neurite bundles innervating the median organ (nm) are detectable in the dorsal part of the brain. The latter bundles branch of from the dorsal root (dr) and run towards the median organ tip, where they terminate in distinct immunoreactive perikarya (arrowheads). At the base of the median organ distinct ciliated tufts (dashed circles) are present. b In pre-metamorphic stages of I. australiensis a comparable situation can be found. In these larvae the neurite innervating the ciliated tufts (dashed circles) branches of from the neurite bundles innervating the median organ (nm). c 26 dpf the bifurcation between (nm) and the neurite running towards the ciliated tuft is obvious. d The neurite bundles innervating the median organ branch off in a region closely related to the dorsal root of the circumesophageal connective (dr) and run towards the median organ tip. A prominent bifurcation (arrowhead) connects the ciliated tufts (dashed circles) with the later bundles. e In post-metamorphic stages the prominent neurite bundles innervating the median organ (nm), the apical immunoreactive perikaya as well as the ciliated tufts (dashed circles) are still present. Note that the entire median organ complex has changed its position during metamorphosis – from a dorsal towards a frontal orientation. br, brain; cc, circumesophageal connective; dr, dorsal root of the circumesophageal connective; nm, neurite bundle innervating the median organ; pl, palps; pn, palp nerve; pt., prototroch; vr, ventral root of the circumesophageal connective. Scale bars = 80 μm (a), 60 μm (b, c) and 30 μm (d, e)
Fig. 4
Fig. 4
Occurrence of myoinhibitory peptide (MIP) in the median organ of Sabellariidae. Confocal maximum projections of α-tub-LIR (white), MIP-LIR (red) and DAPI (blue) staining. Anterior is up in all images. All views are from dorsal, except of (c) and (d) which are apical views. The shape of the median organ is indicated by dashed lines and prominent immunoreactive perikarya are marked with arrowheads. Age of the larvae is given in days post fertilization (dpf) and the species identity as well as the colour code for the shown staining is specified in the respective figure. a Distinct MIP-LIR is exhibited close to the brain (br), at the base of the median organ and along the palps (pl). b The median organ tip exhibits immunoreactive somata as well. c, d An anti-MIP staining without counterstaining illustrates the position of the prominent somata with MIP-LIR at the base of the median organ. br, brain; nm, neurite bundle innervating the median organ; pl, palps; pt., prototroch. Scale bars = 80 μm
Fig. 5
Fig. 5
Semi-thin sections and electron microscopic images of the median organ of adult Sabellaria alveolata. Toluidin-blue staining (a) and electron microscopy (b-e). a An antero-posterior section of the adult median organ (mo) reveals the presence numerous ciliated pits (arrow heads) at the base of the structure. The red dashed squares indicate the position of the images shown in (b) and (e). b A higher magnification of a ciliated pit reveals the presence of numerous ciliated supporting cells (cc) surrounding the epidermal depression, and sending cilia (ci) out of the opening of the pit. A sensory cell (sc) situated near the pit opening sends a distinct cellular process (red arrowheads) towards the epidermal surface. The olfactory chamber (oc) is located in the region where the cellular process reaches the surface. c A close-up supporting cells (cc) present the density of cilia running into the epidermal depression of the pit. d A section showing the inner surface of the pit reveals a dense pattern of cilia (ci) and microvilli. e Close to the pit, but outside the epidermal depression, numerous ciliated supporting cells (cc) cover the epidermal surface. cc, ciliated supporting cell; mo, median organ; sc, sensory cell. Scale bars = 10 μm (b, e), 2 μm (c) and 500 nm (d)
Fig. 6
Fig. 6
Semithin sections and electron microscopic images of the median organ of adult Idanthyrsus australiensis. Toluidin-blue staining (a), HES staining (b-d) and electron microscopy (e-j). a An antero-posterior section of the adult median organ (mo) reveals the presence of numerous ciliated pits bearing ciliary tufts (arrow heads) at the base of the structure. The red dashed squares indicate the position of the images shown in (f) and (e). b An anterior-posterior section at the base of the median organ (mo) exhibits the distinct neurite bundles (nm) innervating the (mo). The red arrow marks the position of ocelli. c The tip of the median organ (mo) possess a dense ciliation (ci) and a prominent nervous system innervation (ns). d Under higher magnification the proximity of photo-sensitive ocelli (red arrows) and the neurite bundles (nm) innervating the (mo) becomes obvious. e An electron microscopic image of the ciliated pit shows presence of numerous ciliated supporting cells (cc) at the base of the epidermal depression and an olfactory chamber (oc) in close proximity. f The area surrounding the ciliary pits is covered with cilia originating from numerous ciliated supporting cells (cc). g A cross section of the inner surface of the ciliated pit reveals a dense mixture of cilia (ci) and microvilli (mv) covering the surface of the supporting cells. h, i An electron microscopic image of the ocelli reveals presence of a pigment cell (pc) and a sensory cell (sc) sending the sensory membrane (sm) towards the pigment cell cup. Note that the pigment granules are not visible due to fixation artefacts. j The rhabdomeric-like sensory membrane can be described as microvillar, but with a whorled appearance. br, brain; cc, ciliated supporting cell; ci, cilia; cu, cuticle; mo, median organ; mv, microvilli; nm, neurite bundle innervating the median organ; ns, nervous system; oc, olfactory chamber; pc, pigment cell forming the pigment cup; sc, sensory cell; sm, sensory membrane. Scale bars = 1 μm (e, g), 5 μm (f, h), 2 μm (i) and 200 nm (j)

Similar articles

See all similar articles

References

    1. Pechenik J. On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles. Mar Ecol Prog Ser. 1999;177:269–297. doi: 10.3354/meps177269. - DOI
    1. Wilson WH. Sexual reproductive modes in Polychaetes: classification and diversity. Bull Mar Sci. 1991;48(2):500–16.
    1. Giangrande A. Polychaete reproductive patterns, life cycles and life histories: an overview. Oceanogr Mar Biol Annu Rev. 1997;35:323–386.
    1. Capa M, Hutchings P. Handbook of zoology. 2014. Sabellariidae Johnston, 1865.
    1. Brinkmann N, Wanninger A. Larval neurogenesis in Sabellaria alveolata reveals plasticity in polychaete neural patterning. Evol Dev. 2008;10:606–618. doi: 10.1111/j.1525-142X.2008.00275.x. - DOI - PubMed

Publication types

LinkOut - more resources

Feedback