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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

Organization of tentacles in competent larvae of Phoronopsis harmeri. Semi-thin cross section (A) and thin cross sections (B-E). (A) Section of the middle part of a tentacle. Around each tentacle, there are several zones of epidermis: frontal (fz), lateral (lz), abfrontal (afz), two laterofrontal (lfz), and two lateroabfrontal (laz). (B) Section of the apical portion of the laterofrontal sensory cell with a cilium (c) and thick microvilli (tm), which are much thicker than regular microvilli (tom). (C) The mediofrontal (at the top) and two laterofrontal (to the sides) neurite bundles (green). A nonsensory perikaryon (pink) is associated with the mediofrontal neurite bundle. (D) Two small lateroabfrontal neurite bundles (green). (E) The portion of the laterofrontal epidermis with the sensory laterofrontal cell (sc), which bears thick microvilli, and an additional sensory cell (blue) that contacts the laterofrontal neurite bundle (green). Abbreviations: afz – abfrontal zone of tentacle; bc – blastocoel; c – cilium; cc – cells of coelomic lining; G – Golgi apparatus; laz – lateroabfrontal zone of tentacle; lf – laterofrontal neurite bundle; lfz – laterofrontal zone of tentacle; lz – lateral zone of tentacle; mc – muscle cells; mf – mediofrontal neurite bundle; n – nucleus; nf – nerve fibers; sc – laterofrontal sensory cell; sr – striated rootlet; tm – thick microvilli, tom – thin microvilli.
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Figure 11: Organization of tentacles in competent larvae of Phoronopsis harmeri. Semi-thin cross section (A) and thin cross sections (B-E). (A) Section of the middle part of a tentacle. Around each tentacle, there are several zones of epidermis: frontal (fz), lateral (lz), abfrontal (afz), two laterofrontal (lfz), and two lateroabfrontal (laz). (B) Section of the apical portion of the laterofrontal sensory cell with a cilium (c) and thick microvilli (tm), which are much thicker than regular microvilli (tom). (C) The mediofrontal (at the top) and two laterofrontal (to the sides) neurite bundles (green). A nonsensory perikaryon (pink) is associated with the mediofrontal neurite bundle. (D) Two small lateroabfrontal neurite bundles (green). (E) The portion of the laterofrontal epidermis with the sensory laterofrontal cell (sc), which bears thick microvilli, and an additional sensory cell (blue) that contacts the laterofrontal neurite bundle (green). Abbreviations: afz – abfrontal zone of tentacle; bc – blastocoel; c – cilium; cc – cells of coelomic lining; G – Golgi apparatus; laz – lateroabfrontal zone of tentacle; lf – laterofrontal neurite bundle; lfz – laterofrontal zone of tentacle; lz – lateral zone of tentacle; mc – muscle cells; mf – mediofrontal neurite bundle; n – nucleus; nf – nerve fibers; sc – laterofrontal sensory cell; sr – striated rootlet; tm – thick microvilli, tom – thin microvilli.

Mentions: In competent larvae, each tentacle has several zones, which differ in the organization of the epidermis (Figure 11A). Each tentacle contains five neurite bundles. The largest bundle is mediofrontal. It consists of 80-100 neurites and is located strictly above the tentacle elevator (Figure 11C). The mediofrontal neurite bundle is closely associated with perikarya, which contain a few clear synaptic vesicles and nuclei with electron-lucent karyoplasm and large nucleoli (Figure 11C). Two laterofrontal neurite bundles are associated with the sensory laterofrontal cells. Each laterofrontal bundle consists of 40-50 neurites (Figure 11C). Sensory cells are arranged along each tentacle in two rows. Each of these cells has a cilium, which is surrounded by eight, thick microvilli (Figure 11B). The basal body of the cilium gives rise to three striated rootlets, which pass along the nucleus (Figure 11E). Common epidermal cells, which are also apparently sensory, occur near typical sensory cells with thick microvilli (Figure 11E). The basal parts of these epidermal cells form projections, which contain synaptic vesicles. Paired lateroabfrontal neurite bundles are usually associated with gland cells. These are the smallest bundles and consist of 15-20 neurites (Figure 11D).


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

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

Organization of tentacles in competent larvae of Phoronopsis harmeri. Semi-thin cross section (A) and thin cross sections (B-E). (A) Section of the middle part of a tentacle. Around each tentacle, there are several zones of epidermis: frontal (fz), lateral (lz), abfrontal (afz), two laterofrontal (lfz), and two lateroabfrontal (laz). (B) Section of the apical portion of the laterofrontal sensory cell with a cilium (c) and thick microvilli (tm), which are much thicker than regular microvilli (tom). (C) The mediofrontal (at the top) and two laterofrontal (to the sides) neurite bundles (green). A nonsensory perikaryon (pink) is associated with the mediofrontal neurite bundle. (D) Two small lateroabfrontal neurite bundles (green). (E) The portion of the laterofrontal epidermis with the sensory laterofrontal cell (sc), which bears thick microvilli, and an additional sensory cell (blue) that contacts the laterofrontal neurite bundle (green). Abbreviations: afz – abfrontal zone of tentacle; bc – blastocoel; c – cilium; cc – cells of coelomic lining; G – Golgi apparatus; laz – lateroabfrontal zone of tentacle; lf – laterofrontal neurite bundle; lfz – laterofrontal zone of tentacle; lz – lateral zone of tentacle; mc – muscle cells; mf – mediofrontal neurite bundle; n – nucleus; nf – nerve fibers; sc – laterofrontal sensory cell; sr – striated rootlet; tm – thick microvilli, tom – thin microvilli.
© Copyright Policy - open-access
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3924620&req=5

Figure 11: Organization of tentacles in competent larvae of Phoronopsis harmeri. Semi-thin cross section (A) and thin cross sections (B-E). (A) Section of the middle part of a tentacle. Around each tentacle, there are several zones of epidermis: frontal (fz), lateral (lz), abfrontal (afz), two laterofrontal (lfz), and two lateroabfrontal (laz). (B) Section of the apical portion of the laterofrontal sensory cell with a cilium (c) and thick microvilli (tm), which are much thicker than regular microvilli (tom). (C) The mediofrontal (at the top) and two laterofrontal (to the sides) neurite bundles (green). A nonsensory perikaryon (pink) is associated with the mediofrontal neurite bundle. (D) Two small lateroabfrontal neurite bundles (green). (E) The portion of the laterofrontal epidermis with the sensory laterofrontal cell (sc), which bears thick microvilli, and an additional sensory cell (blue) that contacts the laterofrontal neurite bundle (green). Abbreviations: afz – abfrontal zone of tentacle; bc – blastocoel; c – cilium; cc – cells of coelomic lining; G – Golgi apparatus; laz – lateroabfrontal zone of tentacle; lf – laterofrontal neurite bundle; lfz – laterofrontal zone of tentacle; lz – lateral zone of tentacle; mc – muscle cells; mf – mediofrontal neurite bundle; n – nucleus; nf – nerve fibers; sc – laterofrontal sensory cell; sr – striated rootlet; tm – thick microvilli, tom – thin microvilli.
Mentions: In competent larvae, each tentacle has several zones, which differ in the organization of the epidermis (Figure 11A). Each tentacle contains five neurite bundles. The largest bundle is mediofrontal. It consists of 80-100 neurites and is located strictly above the tentacle elevator (Figure 11C). The mediofrontal neurite bundle is closely associated with perikarya, which contain a few clear synaptic vesicles and nuclei with electron-lucent karyoplasm and large nucleoli (Figure 11C). Two laterofrontal neurite bundles are associated with the sensory laterofrontal cells. Each laterofrontal bundle consists of 40-50 neurites (Figure 11C). Sensory cells are arranged along each tentacle in two rows. Each of these cells has a cilium, which is surrounded by eight, thick microvilli (Figure 11B). The basal body of the cilium gives rise to three striated rootlets, which pass along the nucleus (Figure 11E). Common epidermal cells, which are also apparently sensory, occur near typical sensory cells with thick microvilli (Figure 11E). The basal parts of these epidermal cells form projections, which contain synaptic vesicles. Paired lateroabfrontal neurite bundles are usually associated with gland cells. These are the smallest bundles and consist of 15-20 neurites (Figure 11D).

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