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Comparative neuroanatomy suggests repeated reduction of neuroarchitectural complexity in Annelida.

Heuer CM, Müller CH, Todt C, Loesel R - Front. Zool. (2010)

Bottom Line: It is concluded that the apparent homology of mushroom bodies in distantly related groups has to be interpreted as a plesiomorphy, pointing towards a considerably complex neuroarchitecture inherited from the last common ancestor, Urbilateria.Within the annelid radiation, the lack of mushroom bodies in certain groups is explained by widespread secondary reductions owing to selective pressures unfavorable for the differentiation of elaborate brains.Evolutionary pathways of mushroom body neuropils in errant polychaetes remain enigmatic.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute for Biology II, RWTH Aachen, Department of Developmental Biology and Morphology of Animals, D-52056 Aachen, Germany. loesel@bio2.rwth-aachen.de.

ABSTRACT

Background: Paired mushroom bodies, an unpaired central complex, and bilaterally arranged clusters of olfactory glomeruli are among the most distinctive components of arthropod neuroarchitecture. Mushroom body neuropils, unpaired midline neuropils, and olfactory glomeruli also occur in the brains of some polychaete annelids, showing varying degrees of morphological similarity to their arthropod counterparts. Attempts to elucidate the evolutionary origin of these neuropils and to deduce an ancestral ground pattern of annelid cerebral complexity are impeded by the incomplete knowledge of annelid phylogeny and by a lack of comparative neuroanatomical data for this group. The present account aims to provide new morphological data for a broad range of annelid taxa in order to trace the occurrence and variability of higher brain centers in segmented worms.

Results: Immunohistochemically stained preparations provide comparative neuroanatomical data for representatives from 22 annelid species. The most prominent neuropil structures to be encountered in the annelid brain are the paired mushroom bodies that occur in a number of polychaete taxa. Mushroom bodies can in some cases be demonstrated to be closely associated with clusters of spheroid neuropils reminiscent of arthropod olfactory glomeruli. Less distinctive subcompartments of the annelid brain are unpaired midline neuropils that bear a remote resemblance to similar components in the arthropod brain. The occurrence of higher brain centers such as mushroom bodies, olfactory glomeruli, and unpaired midline neuropils seems to be restricted to errant polychaetes.

Conclusions: The implications of an assumed homology between annelid and arthropod mushroom bodies are discussed in light of the 'new animal phylogeny'. It is concluded that the apparent homology of mushroom bodies in distantly related groups has to be interpreted as a plesiomorphy, pointing towards a considerably complex neuroarchitecture inherited from the last common ancestor, Urbilateria. Within the annelid radiation, the lack of mushroom bodies in certain groups is explained by widespread secondary reductions owing to selective pressures unfavorable for the differentiation of elaborate brains. Evolutionary pathways of mushroom body neuropils in errant polychaetes remain enigmatic.

No MeSH data available.


Consecutive horizontal sections through the head of Hesione pantherina (proceeding ventrad from a-d). The overlay images show FMRFamide-like immunoreactivity (yellow, left half) and autofluorescence images (red, right half) together with DAPI-labeled cell nuclei (blue). Immunostainings reveal intricate patterns in the dorsal part of the fiber mass (a, b). Paired aggregations of small globuli cells (gc) are situated in front of the anterior eyes (ae) and give rise to stalk-like neuropils converging at the midline of the brain. While the central parts of these neuropils are nearly devoid of immunostaining, scattered FMRFamide-like immunoreactivity can be observed in the peripheral parts (b). Ventrally, the globuli cell mass extends posteriorly, surrounding the central fiber mass, which is now clearly separated into two hemispheres. Small spheroid subcompartments, reminiscent of olfactory glomeruli, can be discerned in the posterior region of each hemisphere (arrowheads). Autofluorescence also reveals a striation of the nervous tissue in the ventral part of the brain. ec circumesophageal connective, p palps, pa prostomial antennae, pe posterior eyes. Scale bar: 80 μm.
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Figure 9: Consecutive horizontal sections through the head of Hesione pantherina (proceeding ventrad from a-d). The overlay images show FMRFamide-like immunoreactivity (yellow, left half) and autofluorescence images (red, right half) together with DAPI-labeled cell nuclei (blue). Immunostainings reveal intricate patterns in the dorsal part of the fiber mass (a, b). Paired aggregations of small globuli cells (gc) are situated in front of the anterior eyes (ae) and give rise to stalk-like neuropils converging at the midline of the brain. While the central parts of these neuropils are nearly devoid of immunostaining, scattered FMRFamide-like immunoreactivity can be observed in the peripheral parts (b). Ventrally, the globuli cell mass extends posteriorly, surrounding the central fiber mass, which is now clearly separated into two hemispheres. Small spheroid subcompartments, reminiscent of olfactory glomeruli, can be discerned in the posterior region of each hemisphere (arrowheads). Autofluorescence also reveals a striation of the nervous tissue in the ventral part of the brain. ec circumesophageal connective, p palps, pa prostomial antennae, pe posterior eyes. Scale bar: 80 μm.

Mentions: Immunohistochemical methods were used to analyze brain anatomy and reveal neuropil substructures in representatives of 22 annelid species(see Table 1). Additionally, immunostained sections of an arthropod brain (Leucophaea maderae, Insecta) are presented for comparative purposes (Fig. 1). A 3D rendering of neuropils encountered in the polychaete Lepidonotus clava is presented in Fig. 2. Figs. 3, 4, 5, and 6 summarize the occurrence and anatomy of distinctive cerebral neuropils across the range of the investigated species. Results are shown in exemplary horizontal sections of immunohistochemical preparations, along with schematic drawings depicting characteristic neuroanatomical features for each of the investigated species. Additional figure plates present neuroanatomical similarities in closely related species (Figs. 7, 8) as well as details on neuropil substructures (Figs. 9, 10, 11).


Comparative neuroanatomy suggests repeated reduction of neuroarchitectural complexity in Annelida.

Heuer CM, Müller CH, Todt C, Loesel R - Front. Zool. (2010)

Consecutive horizontal sections through the head of Hesione pantherina (proceeding ventrad from a-d). The overlay images show FMRFamide-like immunoreactivity (yellow, left half) and autofluorescence images (red, right half) together with DAPI-labeled cell nuclei (blue). Immunostainings reveal intricate patterns in the dorsal part of the fiber mass (a, b). Paired aggregations of small globuli cells (gc) are situated in front of the anterior eyes (ae) and give rise to stalk-like neuropils converging at the midline of the brain. While the central parts of these neuropils are nearly devoid of immunostaining, scattered FMRFamide-like immunoreactivity can be observed in the peripheral parts (b). Ventrally, the globuli cell mass extends posteriorly, surrounding the central fiber mass, which is now clearly separated into two hemispheres. Small spheroid subcompartments, reminiscent of olfactory glomeruli, can be discerned in the posterior region of each hemisphere (arrowheads). Autofluorescence also reveals a striation of the nervous tissue in the ventral part of the brain. ec circumesophageal connective, p palps, pa prostomial antennae, pe posterior eyes. Scale bar: 80 μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2874545&req=5

Figure 9: Consecutive horizontal sections through the head of Hesione pantherina (proceeding ventrad from a-d). The overlay images show FMRFamide-like immunoreactivity (yellow, left half) and autofluorescence images (red, right half) together with DAPI-labeled cell nuclei (blue). Immunostainings reveal intricate patterns in the dorsal part of the fiber mass (a, b). Paired aggregations of small globuli cells (gc) are situated in front of the anterior eyes (ae) and give rise to stalk-like neuropils converging at the midline of the brain. While the central parts of these neuropils are nearly devoid of immunostaining, scattered FMRFamide-like immunoreactivity can be observed in the peripheral parts (b). Ventrally, the globuli cell mass extends posteriorly, surrounding the central fiber mass, which is now clearly separated into two hemispheres. Small spheroid subcompartments, reminiscent of olfactory glomeruli, can be discerned in the posterior region of each hemisphere (arrowheads). Autofluorescence also reveals a striation of the nervous tissue in the ventral part of the brain. ec circumesophageal connective, p palps, pa prostomial antennae, pe posterior eyes. Scale bar: 80 μm.
Mentions: Immunohistochemical methods were used to analyze brain anatomy and reveal neuropil substructures in representatives of 22 annelid species(see Table 1). Additionally, immunostained sections of an arthropod brain (Leucophaea maderae, Insecta) are presented for comparative purposes (Fig. 1). A 3D rendering of neuropils encountered in the polychaete Lepidonotus clava is presented in Fig. 2. Figs. 3, 4, 5, and 6 summarize the occurrence and anatomy of distinctive cerebral neuropils across the range of the investigated species. Results are shown in exemplary horizontal sections of immunohistochemical preparations, along with schematic drawings depicting characteristic neuroanatomical features for each of the investigated species. Additional figure plates present neuroanatomical similarities in closely related species (Figs. 7, 8) as well as details on neuropil substructures (Figs. 9, 10, 11).

Bottom Line: It is concluded that the apparent homology of mushroom bodies in distantly related groups has to be interpreted as a plesiomorphy, pointing towards a considerably complex neuroarchitecture inherited from the last common ancestor, Urbilateria.Within the annelid radiation, the lack of mushroom bodies in certain groups is explained by widespread secondary reductions owing to selective pressures unfavorable for the differentiation of elaborate brains.Evolutionary pathways of mushroom body neuropils in errant polychaetes remain enigmatic.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute for Biology II, RWTH Aachen, Department of Developmental Biology and Morphology of Animals, D-52056 Aachen, Germany. loesel@bio2.rwth-aachen.de.

ABSTRACT

Background: Paired mushroom bodies, an unpaired central complex, and bilaterally arranged clusters of olfactory glomeruli are among the most distinctive components of arthropod neuroarchitecture. Mushroom body neuropils, unpaired midline neuropils, and olfactory glomeruli also occur in the brains of some polychaete annelids, showing varying degrees of morphological similarity to their arthropod counterparts. Attempts to elucidate the evolutionary origin of these neuropils and to deduce an ancestral ground pattern of annelid cerebral complexity are impeded by the incomplete knowledge of annelid phylogeny and by a lack of comparative neuroanatomical data for this group. The present account aims to provide new morphological data for a broad range of annelid taxa in order to trace the occurrence and variability of higher brain centers in segmented worms.

Results: Immunohistochemically stained preparations provide comparative neuroanatomical data for representatives from 22 annelid species. The most prominent neuropil structures to be encountered in the annelid brain are the paired mushroom bodies that occur in a number of polychaete taxa. Mushroom bodies can in some cases be demonstrated to be closely associated with clusters of spheroid neuropils reminiscent of arthropod olfactory glomeruli. Less distinctive subcompartments of the annelid brain are unpaired midline neuropils that bear a remote resemblance to similar components in the arthropod brain. The occurrence of higher brain centers such as mushroom bodies, olfactory glomeruli, and unpaired midline neuropils seems to be restricted to errant polychaetes.

Conclusions: The implications of an assumed homology between annelid and arthropod mushroom bodies are discussed in light of the 'new animal phylogeny'. It is concluded that the apparent homology of mushroom bodies in distantly related groups has to be interpreted as a plesiomorphy, pointing towards a considerably complex neuroarchitecture inherited from the last common ancestor, Urbilateria. Within the annelid radiation, the lack of mushroom bodies in certain groups is explained by widespread secondary reductions owing to selective pressures unfavorable for the differentiation of elaborate brains. Evolutionary pathways of mushroom body neuropils in errant polychaetes remain enigmatic.

No MeSH data available.