Differential involvement of Hedgehog signaling in butterfly wing and eyespot development.

Butterfly eyespots may have evolved from the recruitment of pre-existent gene circuits or regulatory networks into novel locations on the wing. Gene expression data suggests one such circuit, the Hedgehog (Hh) signaling pathway and its target gene engrailed (en), was recruited from a role in pattern...

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Autores principales: Xiaoling Tong, Anna Lindemann, Antónia Monteiro
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Publicado: Public Library of Science (PLoS) 2012
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Acceso en línea:https://doaj.org/article/bb1dab6793804d07b0e776f039733dce
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spelling oai:doaj.org-article:bb1dab6793804d07b0e776f039733dce2021-11-18T08:06:14ZDifferential involvement of Hedgehog signaling in butterfly wing and eyespot development.1932-620310.1371/journal.pone.0051087https://doaj.org/article/bb1dab6793804d07b0e776f039733dce2012-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23227236/?tool=EBIhttps://doaj.org/toc/1932-6203Butterfly eyespots may have evolved from the recruitment of pre-existent gene circuits or regulatory networks into novel locations on the wing. Gene expression data suggests one such circuit, the Hedgehog (Hh) signaling pathway and its target gene engrailed (en), was recruited from a role in patterning the anterior-posterior insect wing axis to a role patterning butterfly eyespots. However, while Junonia coenia expresses hh and en both in the posterior compartment of the wing and in eyespot centers, Bicyclus anynana lacks hh eyespot-specific expression. This suggests that Hh signaling may not be functioning in eyespot development in either species or that it functions in J. coenia but not in B. anynana. In order to test these hypotheses, we performed functional tests of Hh signaling in these species. We investigated the effects of Hh protein sequestration during the larval stage on en expression levels, and on wing size and eyespot size in adults. Hh sequestration led to significantly reduced en expression and to significantly smaller wings and eyespots in both species. But while eyespot size in B. anynana was reduced proportionately to wing size, in J. coenia, eyespots were reduced disproportionately, indicating an independent role of Hh signaling in eyespot development in J. coenia. We conclude that while Hh signaling retains a conserved role in promoting wing growth across nymphalid butterflies, it plays an additional role in eyespot development in some, but not all, lineages of nymphalid butterflies. We discuss our findings in the context of alternative evolutionary scenarios that led to the differential expression of hh and other Hh pathway signaling members across nymphalid species.Xiaoling TongAnna LindemannAntónia MonteiroPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 7, Iss 12, p e51087 (2012)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Xiaoling Tong
Anna Lindemann
Antónia Monteiro
Differential involvement of Hedgehog signaling in butterfly wing and eyespot development.
description Butterfly eyespots may have evolved from the recruitment of pre-existent gene circuits or regulatory networks into novel locations on the wing. Gene expression data suggests one such circuit, the Hedgehog (Hh) signaling pathway and its target gene engrailed (en), was recruited from a role in patterning the anterior-posterior insect wing axis to a role patterning butterfly eyespots. However, while Junonia coenia expresses hh and en both in the posterior compartment of the wing and in eyespot centers, Bicyclus anynana lacks hh eyespot-specific expression. This suggests that Hh signaling may not be functioning in eyespot development in either species or that it functions in J. coenia but not in B. anynana. In order to test these hypotheses, we performed functional tests of Hh signaling in these species. We investigated the effects of Hh protein sequestration during the larval stage on en expression levels, and on wing size and eyespot size in adults. Hh sequestration led to significantly reduced en expression and to significantly smaller wings and eyespots in both species. But while eyespot size in B. anynana was reduced proportionately to wing size, in J. coenia, eyespots were reduced disproportionately, indicating an independent role of Hh signaling in eyespot development in J. coenia. We conclude that while Hh signaling retains a conserved role in promoting wing growth across nymphalid butterflies, it plays an additional role in eyespot development in some, but not all, lineages of nymphalid butterflies. We discuss our findings in the context of alternative evolutionary scenarios that led to the differential expression of hh and other Hh pathway signaling members across nymphalid species.
format article
author Xiaoling Tong
Anna Lindemann
Antónia Monteiro
author_facet Xiaoling Tong
Anna Lindemann
Antónia Monteiro
author_sort Xiaoling Tong
title Differential involvement of Hedgehog signaling in butterfly wing and eyespot development.
title_short Differential involvement of Hedgehog signaling in butterfly wing and eyespot development.
title_full Differential involvement of Hedgehog signaling in butterfly wing and eyespot development.
title_fullStr Differential involvement of Hedgehog signaling in butterfly wing and eyespot development.
title_full_unstemmed Differential involvement of Hedgehog signaling in butterfly wing and eyespot development.
title_sort differential involvement of hedgehog signaling in butterfly wing and eyespot development.
publisher Public Library of Science (PLoS)
publishDate 2012
url https://doaj.org/article/bb1dab6793804d07b0e776f039733dce
work_keys_str_mv AT xiaolingtong differentialinvolvementofhedgehogsignalinginbutterflywingandeyespotdevelopment
AT annalindemann differentialinvolvementofhedgehogsignalinginbutterflywingandeyespotdevelopment
AT antoniamonteiro differentialinvolvementofhedgehogsignalinginbutterflywingandeyespotdevelopment
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