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Development and organization of the larval nervous system in Phoronopsis harmeri: new insights into phoronid phylogeny.

Temereva EN, Tsitrin EB - Front. Zool. (2014)

Bottom Line: Phoronid larvae demonstrate some "deuterostome-like" features, which are, in fact, have to be ancestral bilaterian characters.Our new results and previous data indicate that phoronids have retained some plesiomorphic features, which were inherited from the last common ancestor of all Bilateria.It follows that phoronids should be extracted from the Trochozoan (=Spiralia) clade and placed at the base of the Lophotrochozoan stem.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Invertebrate Zoology, Biological faculty, Moscow State University, Moscow 119992, Russia. temereva@mail.ru.

ABSTRACT

Background: The organization and development of the nervous system has traditionally been used as an important character for establishing the relationships among large groups of animals. According to this criterion, phoronids were initially regarded as deuterostomian but have more recently been regarded as protostomian. The resolving of this conflict requires detailed information from poorly investigated members of phoronids, such as Phoronopsis harmeri.

Results: The serotonin-like immunoreactive part of the P. harmeri nervous system changes during larval development. These changes mostly concern the nervous system of the hood and correlate with the appearance of the median and two marginal neurite bundles, the frontal organ, and the sensory field. The apical organ has bilateral symmetry. The tentacular neurite bundle passes under the tentacles, contains several types of perikarya, and gives rise to intertentacular bundles, which branch in the tentacle base and penetrate into adjacent tentacles by two lateroabfrontal bundles. There are two groups of dorsolateral perikarya, which exhibit serotonin-like immunoreactivity, contact the tentacular neurite bundle, and are located near the youngest tentacles. Larvae have a minor nerve ring, which originates from the posterior marginal neurite bundle of the hood, passes above the tentacle base, and gives rise to the mediofrontal neurite bundle in each tentacle. Paired laterofrontal neurite bundles of tentacles form a continuous nerve tract that conducts to the postoral ciliated band.

Discussion: The organization of the nervous system differs among the planktotrophic larvae of phoronid species. These differences may correlate with differences in phoronid biology. Data concerning the innervation of tentacles in different phoronid larvae are conflicting and require careful reinvestigation. The overall organization of the nervous system in phoronid larvae has more in common with the deuterostomian than with the protostomian nervous system. Phoronid larvae demonstrate some "deuterostome-like" features, which are, in fact, have to be ancestral bilaterian characters. Our new results and previous data indicate that phoronids have retained some plesiomorphic features, which were inherited from the last common ancestor of all Bilateria. It follows that phoronids should be extracted from the Trochozoan (=Spiralia) clade and placed at the base of the Lophotrochozoan stem.

No MeSH data available.


Related in: MedlinePlus

Serotonin-like immunoreactive nervous system in young larvae of Phoronopsis harmeri. In all images, the apical is at the top, except in C where the apical is to the upper right corner. Z-projections (B, C, E-J) of larvae after mono- and double staining for 5-HT (serotonin) (yellow), phalloidin (blue), and alpha-tubulin (cyan). (A) Larva with 18 tentacles (SEM); dorsolateral view. (B) The apical organ viewed from the dorsal side. (C) Dorsal view of larva with 18 tentacles. (D) Live larva with 20 tentacles; ventrolateral view. (E) Perikaryon with cilium and basal process (p) in the apical organ. (F) Dorsal view of the anterior portion of larva with 20 tentacles. (G) Dorsal view of larva with 20 tentacles. (H) Lateral view of the youngest tentacles: the perikarya of dorsolateral group are indicated by arrowheads. (I) Dorsal view of two groups of perikarya (arrowheads), which are located near the youngest tentacles. (J) Lateral view of the anterior portion of larva with 20 tentacles. Abbreviations: am – anterior marginal neurite bundle; ao – apical organ; bm – blood mass; dlp – dorsolateral perikarya; itb – intertentacular branch; la – lateroabfrontal neurites in the tentacle; lp – lower portion of the neuropil of the apical organ; mn – median neurite bundle; ms – metasomal sac; pl – preoral lobe; pm – posterior marginal neurite bundle; t – tentacle; tn – tentacular nerve ring; tr – trunk; tt – telotroch; ttn – telotroch nerve ring; v - varicose (node); up – upper portion of the neuropil of the apical organ; yt – youngest tentacles.
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Figure 1: Serotonin-like immunoreactive nervous system in young larvae of Phoronopsis harmeri. In all images, the apical is at the top, except in C where the apical is to the upper right corner. Z-projections (B, C, E-J) of larvae after mono- and double staining for 5-HT (serotonin) (yellow), phalloidin (blue), and alpha-tubulin (cyan). (A) Larva with 18 tentacles (SEM); dorsolateral view. (B) The apical organ viewed from the dorsal side. (C) Dorsal view of larva with 18 tentacles. (D) Live larva with 20 tentacles; ventrolateral view. (E) Perikaryon with cilium and basal process (p) in the apical organ. (F) Dorsal view of the anterior portion of larva with 20 tentacles. (G) Dorsal view of larva with 20 tentacles. (H) Lateral view of the youngest tentacles: the perikarya of dorsolateral group are indicated by arrowheads. (I) Dorsal view of two groups of perikarya (arrowheads), which are located near the youngest tentacles. (J) Lateral view of the anterior portion of larva with 20 tentacles. Abbreviations: am – anterior marginal neurite bundle; ao – apical organ; bm – blood mass; dlp – dorsolateral perikarya; itb – intertentacular branch; la – lateroabfrontal neurites in the tentacle; lp – lower portion of the neuropil of the apical organ; mn – median neurite bundle; ms – metasomal sac; pl – preoral lobe; pm – posterior marginal neurite bundle; t – tentacle; tn – tentacular nerve ring; tr – trunk; tt – telotroch; ttn – telotroch nerve ring; v - varicose (node); up – upper portion of the neuropil of the apical organ; yt – youngest tentacles.

Mentions: Larvae of P. harmeri are very abundant in the fall in Vostok Bay, the Sea of Japan, and plankton samples contain P. harmeri larvae of different stages. The body of the phoronid larva at different stages is divided into three parts: the preoral lobe (the hood), the collar region with oral field and tentacles, and the trunk. The edge of the hood bears the preoral ciliated band. The postoral ciliated band passes along the laterofrontal sides of the tentacles. The telotroch is located terminally on the trunk and surrounds the anus. The metasomal sac is the invagination of the ventral epidermis under the tentacles. The metasomal sac is located in the trunk coelom and grows with age. Larval stages differ from each other in body size and proportions of body parts; number of tentacles; the presence, number, and color of the blood masses; and the volume of the metasomal sac. The youngest larvae studied here are 600 μm long and have 18 tentacles and lack blood masses (Figure 1A). Larvae with 20 tentacles are 900 μm long and have a tube-like metasomal sac and a pair of dorsolateral blood masses, which are colorless and small in diameter (Figure 1D). Larvae of the next stage are 1200 μm long and have 22 tentacles, a pair of large pale pink blood masses, a looped metasomal sac, and two prominent septa of the stomach (Figure 2A). Competent larvae are 1500 μm long and have 24 tentacles, a pair of large red blood masses on the dorsolateral sides, and 1 to 3 additional small blood masses, which are located in the blastocoel above the tentacles. The metasomal sac of competent larvae occupies most of the trunk coelom. On the ventro-lateral sides, the edge of the preoral lobe is subdivided into two parts: external and internal (Figure 3A). The telotroch of competent larvae is very large and bore numerous long cilia.


Development and organization of the larval nervous system in Phoronopsis harmeri: new insights into phoronid phylogeny.

Temereva EN, Tsitrin EB - Front. Zool. (2014)

Serotonin-like immunoreactive nervous system in young larvae of Phoronopsis harmeri. In all images, the apical is at the top, except in C where the apical is to the upper right corner. Z-projections (B, C, E-J) of larvae after mono- and double staining for 5-HT (serotonin) (yellow), phalloidin (blue), and alpha-tubulin (cyan). (A) Larva with 18 tentacles (SEM); dorsolateral view. (B) The apical organ viewed from the dorsal side. (C) Dorsal view of larva with 18 tentacles. (D) Live larva with 20 tentacles; ventrolateral view. (E) Perikaryon with cilium and basal process (p) in the apical organ. (F) Dorsal view of the anterior portion of larva with 20 tentacles. (G) Dorsal view of larva with 20 tentacles. (H) Lateral view of the youngest tentacles: the perikarya of dorsolateral group are indicated by arrowheads. (I) Dorsal view of two groups of perikarya (arrowheads), which are located near the youngest tentacles. (J) Lateral view of the anterior portion of larva with 20 tentacles. Abbreviations: am – anterior marginal neurite bundle; ao – apical organ; bm – blood mass; dlp – dorsolateral perikarya; itb – intertentacular branch; la – lateroabfrontal neurites in the tentacle; lp – lower portion of the neuropil of the apical organ; mn – median neurite bundle; ms – metasomal sac; pl – preoral lobe; pm – posterior marginal neurite bundle; t – tentacle; tn – tentacular nerve ring; tr – trunk; tt – telotroch; ttn – telotroch nerve ring; v - varicose (node); up – upper portion of the neuropil of the apical organ; yt – youngest tentacles.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
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Figure 1: Serotonin-like immunoreactive nervous system in young larvae of Phoronopsis harmeri. In all images, the apical is at the top, except in C where the apical is to the upper right corner. Z-projections (B, C, E-J) of larvae after mono- and double staining for 5-HT (serotonin) (yellow), phalloidin (blue), and alpha-tubulin (cyan). (A) Larva with 18 tentacles (SEM); dorsolateral view. (B) The apical organ viewed from the dorsal side. (C) Dorsal view of larva with 18 tentacles. (D) Live larva with 20 tentacles; ventrolateral view. (E) Perikaryon with cilium and basal process (p) in the apical organ. (F) Dorsal view of the anterior portion of larva with 20 tentacles. (G) Dorsal view of larva with 20 tentacles. (H) Lateral view of the youngest tentacles: the perikarya of dorsolateral group are indicated by arrowheads. (I) Dorsal view of two groups of perikarya (arrowheads), which are located near the youngest tentacles. (J) Lateral view of the anterior portion of larva with 20 tentacles. Abbreviations: am – anterior marginal neurite bundle; ao – apical organ; bm – blood mass; dlp – dorsolateral perikarya; itb – intertentacular branch; la – lateroabfrontal neurites in the tentacle; lp – lower portion of the neuropil of the apical organ; mn – median neurite bundle; ms – metasomal sac; pl – preoral lobe; pm – posterior marginal neurite bundle; t – tentacle; tn – tentacular nerve ring; tr – trunk; tt – telotroch; ttn – telotroch nerve ring; v - varicose (node); up – upper portion of the neuropil of the apical organ; yt – youngest tentacles.
Mentions: Larvae of P. harmeri are very abundant in the fall in Vostok Bay, the Sea of Japan, and plankton samples contain P. harmeri larvae of different stages. The body of the phoronid larva at different stages is divided into three parts: the preoral lobe (the hood), the collar region with oral field and tentacles, and the trunk. The edge of the hood bears the preoral ciliated band. The postoral ciliated band passes along the laterofrontal sides of the tentacles. The telotroch is located terminally on the trunk and surrounds the anus. The metasomal sac is the invagination of the ventral epidermis under the tentacles. The metasomal sac is located in the trunk coelom and grows with age. Larval stages differ from each other in body size and proportions of body parts; number of tentacles; the presence, number, and color of the blood masses; and the volume of the metasomal sac. The youngest larvae studied here are 600 μm long and have 18 tentacles and lack blood masses (Figure 1A). Larvae with 20 tentacles are 900 μm long and have a tube-like metasomal sac and a pair of dorsolateral blood masses, which are colorless and small in diameter (Figure 1D). Larvae of the next stage are 1200 μm long and have 22 tentacles, a pair of large pale pink blood masses, a looped metasomal sac, and two prominent septa of the stomach (Figure 2A). Competent larvae are 1500 μm long and have 24 tentacles, a pair of large red blood masses on the dorsolateral sides, and 1 to 3 additional small blood masses, which are located in the blastocoel above the tentacles. The metasomal sac of competent larvae occupies most of the trunk coelom. On the ventro-lateral sides, the edge of the preoral lobe is subdivided into two parts: external and internal (Figure 3A). The telotroch of competent larvae is very large and bore numerous long cilia.

Bottom Line: Phoronid larvae demonstrate some "deuterostome-like" features, which are, in fact, have to be ancestral bilaterian characters.Our new results and previous data indicate that phoronids have retained some plesiomorphic features, which were inherited from the last common ancestor of all Bilateria.It follows that phoronids should be extracted from the Trochozoan (=Spiralia) clade and placed at the base of the Lophotrochozoan stem.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Invertebrate Zoology, Biological faculty, Moscow State University, Moscow 119992, Russia. temereva@mail.ru.

ABSTRACT

Background: The organization and development of the nervous system has traditionally been used as an important character for establishing the relationships among large groups of animals. According to this criterion, phoronids were initially regarded as deuterostomian but have more recently been regarded as protostomian. The resolving of this conflict requires detailed information from poorly investigated members of phoronids, such as Phoronopsis harmeri.

Results: The serotonin-like immunoreactive part of the P. harmeri nervous system changes during larval development. These changes mostly concern the nervous system of the hood and correlate with the appearance of the median and two marginal neurite bundles, the frontal organ, and the sensory field. The apical organ has bilateral symmetry. The tentacular neurite bundle passes under the tentacles, contains several types of perikarya, and gives rise to intertentacular bundles, which branch in the tentacle base and penetrate into adjacent tentacles by two lateroabfrontal bundles. There are two groups of dorsolateral perikarya, which exhibit serotonin-like immunoreactivity, contact the tentacular neurite bundle, and are located near the youngest tentacles. Larvae have a minor nerve ring, which originates from the posterior marginal neurite bundle of the hood, passes above the tentacle base, and gives rise to the mediofrontal neurite bundle in each tentacle. Paired laterofrontal neurite bundles of tentacles form a continuous nerve tract that conducts to the postoral ciliated band.

Discussion: The organization of the nervous system differs among the planktotrophic larvae of phoronid species. These differences may correlate with differences in phoronid biology. Data concerning the innervation of tentacles in different phoronid larvae are conflicting and require careful reinvestigation. The overall organization of the nervous system in phoronid larvae has more in common with the deuterostomian than with the protostomian nervous system. Phoronid larvae demonstrate some "deuterostome-like" features, which are, in fact, have to be ancestral bilaterian characters. Our new results and previous data indicate that phoronids have retained some plesiomorphic features, which were inherited from the last common ancestor of all Bilateria. It follows that phoronids should be extracted from the Trochozoan (=Spiralia) clade and placed at the base of the Lophotrochozoan stem.

No MeSH data available.


Related in: MedlinePlus