Future research directions of the model marine tubeworm Hydroides elegans and synthesis of developmental staging of the complete life cycle

Abstract

Background: The biofouling marine tube worm, Hydroides elegans, is an indirect developing polychaete with significance as a model organism for questions in developmental biology and the evolution of host-microbe interactions. However, a complete description of the life cycle from fertilization through sexual maturity remains scattered in the literature, and lacks standardization.

Results and discussion: Here, we present a unified staging scheme synthesizing the major morphological changes that occur during the entire life cycle of the animal. These data represent a complete record of the life cycle, and serve as a foundation for connecting molecular changes with morphology.

Conclusions: The present synthesis and associated staging scheme are especially timely as this system gains traction within research communities. Characterizing the Hydroides life cycle is essential for investigating the molecular mechanisms that drive major developmental transitions, like metamorphosis, in response to bacteria.

Keywords: Hydroides elegans; bacteria; development; metamorphosis.

Figure 1.

Hydroides morphology and life cycle. A) Sexually mature adult dissected out of the calcareous tube. Labelling: ab=abdomen, bc=branchial crown, c=collar, op=operculum, pd=peduncle, pg=pygidium, r=radiole, th=thorax. B) Illustration of the major life history stages in the biphasic life cycle of Hydroides elegans. Metamorphosis is induced by interaction with single- or multi-species biofilms. Scale = 1mm

Figure 2.

Gametes and zygote of Hydroides elegans. A) Sperm. Scale=5μm. B) Unfertilized egg. Scale=10μm. C) Zygote. No obvious morphological changes occur between the oocyte and the zygote. Scale=10μm

Figure 3.

Embryonic cleavage stages in Hydroides elegans. All panels are depicted with the animal pole of the embryo pointing out of the page, and the vegetal pole pointing in to the page. Panels A-B and E-F are single equatorial focal planes. Panels C-D are composite images from multiple focal planes. A) 2-cell embryo. B) 4-cell embryo. C) 8-cell embryo. D) 16-cell embryo. The vegetal blastomeres are not in view. E) 32-cell embryo. F) 60-cell embryo. All panels scale=10μm

Figure 4.

Gastrulation and larval stages in Hydroides elegans. A) Ciliated blastula. Dashed white line outlines the blastocoel. B) Mid-gastrula, oral side of the animal is pointing down. White arrows indicate ciliated cells of the developing prototroch. C) Late gastrula, hatched. White arrows mark ciliated cells of the developing prototroch. Yellow arrow indicates cilia of the apical tuft. D) Lateral view of a feeding trochophore larva. E) Aboral view of a segmented nectochaete larva. F) Oral view of a metamorphically competent larva. Labelling for panels D-F: at=apical tuft, aso=apical sensory organ, av=anal vacuole, ch=newly formed chaetae, col=collar, e=eye spot, it=intestinal tract, m=mouth, mt=metatroch, pt=prototroch, s=larval segments with chaetae, st=stomach. For panels A-C scale=10μm, for panels D-F scale=50μm. Panels D-F are from composite images from multiple focal planes

Figure 5.

Morphological changes associated with bacteria-stimulated metamorphosis in Hydroides elegans. A) Attachment to substrate. B) Formation of the primary tube (indicated by a dashed white line on one side of the larva). C) Shedding of prototroch cilia (*). D) Collar eversion (arrow). E) Shedding of food groove cells (arrow). F) Beginning of lobe formation (dashed white line). G) Lateral extension and elaboration of anterior lobes. H) Juvenile at 24 hours post-metamorphosis. I) Juvenile at 1 week post metamorphosis. Inset of head and elaboration of branchial crown. For panels A-H, scale = 50 μm. For panel I, scale = 250 μm, inset scale = 100 μm

Figure 6.

Summary of Hydroides development from fertilization through sexual maturation. Major phases of development are labelled with individual stages. Images are not to scale. Metamorphosis stages are labelled M1-M7 and correspond to attachment to substrate (M1), formation of the primary tube (M2), shedding of prototroch cilia (M3), collar eversion (M4), shedding of food groove cells (M5), beginning of lobe formation (M6), lateral extension and elaboration of anterior lobes (M7)