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Andreas Hejnol
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ORCiD: https://orcid.org/0000-0003-2196-8507
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Background: Phoronida is a small group of marine worm-like suspension feeders, which together with brachiopods and bryozoans form the clade Lophophorata. Although their development is well studied on the morphological level, data regarding gene expression during this process are scarce and restricted to the analysis of relatively few transcription factors. Here we present a description of the expression patterns of Hox genes during the embryonic and larval development of the phoronid Phoronopsis harmeri. Results: We identified sequences of eight Hox genes in the transcriptome of Ph. harmeri and determined their expression pattern during embryonic and larval development using whole mount in situ hybridization. We found that none of the Hox genes is expressed during embryonic development. Instead their expression is initiated in the later developmental stages, when the larval body is already formed. In the investigated initial larval stages the Hox genes are expressed in the non-collinear manner in the posterior body of the larvae: in the telotroch and the structures that represent rudiments of the adult worm. Additionally, we found that certain head-specific transcription factors are expressed in the oral hood, apical organ, preoral coelom, anterior digestive system and developing larval tentacles, anterior to the Hox-expressing territories. Conclusions: The lack of Hox gene expression during early development of Ph. harmeri indicates that the larval body develops without positional information from the Hox patterning system. Such phenomenon might be a consequence of the evolutionary intercalation of the larval form into an ancestral life cycle of phoronids. The observed Hox gene expression can also be a consequence of the actinotrocha representing a “head larva”, which is composed of the most anterior body region that is devoid of Hox gene expression. Such interpretation is further supported by the expression of head-specific transcription factors. This implies that the Hox patterning system is used for the positional information of the trunk rudiments and is, therefore, delayed to the later larval stages. We propose that a new body form was intercalated to the phoronid life cycle by precocious development of the anterior structures or by delayed development of the trunk rudiment in the ancestral phoronid larva.
Keywords
Lophophorata, Spiralia, biphasic life cycle, intercalation, life history evolution, body plan, indirect development, Lox2, head, brain
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On 28 Jan, 2020
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On 27 Jan, 2020
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Review #3 received
Received 13 Dec, 2019
Editorial decision: Minor revision
On 13 Dec, 2019
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Received 07 Dec, 2019
Review #2 received
Received 07 Dec, 2019
Reviewer #3 agreed
On 02 Dec, 2019
Editor assigned
On 27 Nov, 2019
Reviewers invited
Invitations sent on 27 Nov, 2019
Reviewer #1 agreed
On 27 Nov, 2019
Reviewer #2 agreed
On 27 Nov, 2019
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This preprint is under consideration at EvoDevo. A preprint is a preliminary version of a manuscript that has not completed peer review at a journal. Research Square does not conduct peer review prior to posting preprints. The posting of a preprint on this server should not be interpreted as an endorsement of its validity or suitability for dissemination as established information or for guiding clinical practice.
Learn more about In Review
Research
Andreas Hejnol
Corresponding Author
ORCiD: https://orcid.org/0000-0003-2196-8507
Badges
Prescreen
This manuscript passed our Prescreen assessment
Complete author information
Appropriate declaration statements
Potential risks to human health
Prescreen
Peer Review Timeline
CURRENT STATUS: Published
Version 2
Posted 29 Jan, 2020
Published
On 10 Feb, 2020
No community comments so far
Editor assigned
On 28 Jan, 2020
Editorial decision: Accept
On 28 Jan, 2020
Submission checks complete
On 27 Jan, 2020
Editor invited
On 27 Jan, 2020
No comments provided
Review #3 received
Received 13 Dec, 2019
Editorial decision: Minor revision
On 13 Dec, 2019
Review #1 received
Received 07 Dec, 2019
Review #2 received
Received 07 Dec, 2019
Reviewer #3 agreed
On 02 Dec, 2019
Editor assigned
On 27 Nov, 2019
Reviewers invited
Invitations sent on 27 Nov, 2019
Reviewer #1 agreed
On 27 Nov, 2019
Reviewer #2 agreed
On 27 Nov, 2019
First submitted
On 26 Nov, 2019
Submission checks complete
On 26 Nov, 2019
Editor invited
On 26 Nov, 2019
Metrics
Comments: 0
PDF Downloads: ...
HTML Views: ...
License:
This work is licensed under a CC BY 4.0 License. Read Full License
View the published article at EvoDevo.
Background: Phoronida is a small group of marine worm-like suspension feeders, which together with brachiopods and bryozoans form the clade Lophophorata. Although their development is well studied on the morphological level, data regarding gene expression during this process are scarce and restricted to the analysis of relatively few transcription factors. Here we present a description of the expression patterns of Hox genes during the embryonic and larval development of the phoronid Phoronopsis harmeri. Results: We identified sequences of eight Hox genes in the transcriptome of Ph. harmeri and determined their expression pattern during embryonic and larval development using whole mount in situ hybridization. We found that none of the Hox genes is expressed during embryonic development. Instead their expression is initiated in the later developmental stages, when the larval body is already formed. In the investigated initial larval stages the Hox genes are expressed in the non-collinear manner in the posterior body of the larvae: in the telotroch and the structures that represent rudiments of the adult worm. Additionally, we found that certain head-specific transcription factors are expressed in the oral hood, apical organ, preoral coelom, anterior digestive system and developing larval tentacles, anterior to the Hox-expressing territories. Conclusions: The lack of Hox gene expression during early development of Ph. harmeri indicates that the larval body develops without positional information from the Hox patterning system. Such phenomenon might be a consequence of the evolutionary intercalation of the larval form into an ancestral life cycle of phoronids. The observed Hox gene expression can also be a consequence of the actinotrocha representing a “head larva”, which is composed of the most anterior body region that is devoid of Hox gene expression. Such interpretation is further supported by the expression of head-specific transcription factors. This implies that the Hox patterning system is used for the positional information of the trunk rudiments and is, therefore, delayed to the later larval stages. We propose that a new body form was intercalated to the phoronid life cycle by precocious development of the anterior structures or by delayed development of the trunk rudiment in the ancestral phoronid larva.
Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
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