A Novel Expression Domain of extradenticle Underlies the Evolutionary Developmental Origin of the Chelicerate Patella
- Autores
- Klementz, Benjamin C; Brenneis, Georg; Hinne, Isaac A.; Laumer, Ethan M.; Neu, Sophie M.; Hareid, Grace M.; Gainett, Guilherme; Setton, Emily V. W.; Simian, Catalina; Vrech, David Eduardo; Joyce, Isabella; Barnett, Austen A.; Patel, Nipam H.; Harvey, Mark S.; Peretti, Alfredo Vicente; Gulia Nuss, Monika; Sharma, Prashant P
- Año de publicación
- 2024
- Idioma
- inglés
- Tipo de recurso
- artículo
- Estado
- versión publicada
- Descripción
- Neofunctionalization of duplicated gene copies is thought to be an important process underlying the origin of evolutionary novelty and provides an elegant mechanism for the origin of new phenotypic traits. One putative case where a new gene copy has been linked to a novel morphological trait is the origin of the arachnid patella, a taxonomically restricted leg segment. In spiders, the origin of this segment has been linked to the origin of the paralog dachshund-2, suggesting that a new gene facilitated the expression of a new trait. However, various arachnid groups that possess patellae do not have a copy of dachshund-2, disfavoring the direct link between gene origin and trait origin. We investigated the developmental genetic basis for patellar patterning in the harvestman Phalangium opilio, which lacks dachshund-2. Here, we show that the harvestman patella is established by a novel expression domain of the transcription factor extradenticle. Leveraging this definition of patellar identity, we surveyed targeted groups across chelicerate phylogeny to assess when this trait evolved. We show that a patellar homolog is present in Pycnogonida (sea spiders) and various arachnid orders, suggesting a single origin of the patella in the ancestor of Chelicerata. A potential loss of the patella is observed in Ixodida. Our results suggest that the modification of an ancient gene, rather than the neofunctionalization of a new gene copy, underlies the origin of the patella. Broadly, this work underscores the value of comparative data and broad taxonomic sampling when testing hypotheses in evolutionary developmental biology.
Fil: Klementz, Benjamin C. University of Wisconsin; Estados Unidos
Fil: Brenneis, Georg. Universidad de Viena; Austria
Fil: Hinne, Isaac A.. University Of Nevada; Estados Unidos
Fil: Laumer, Ethan M.. University of Wisconsin; Estados Unidos
Fil: Neu, Sophie M.. University of Wisconsin; Estados Unidos
Fil: Hareid, Grace M.. University of Wisconsin; Estados Unidos
Fil: Gainett, Guilherme. Harvard Medical School; Estados Unidos. University of Wisconsin; Estados Unidos. Boston Children,’s Hospital; Estados Unidos
Fil: Setton, Emily V. W.. Cornell University. Department Of Ecology And Evolutionary Biology; . University of Wisconsin; Estados Unidos
Fil: Simian, Catalina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto de Diversidad y Ecología Animal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto de Diversidad y Ecología Animal; Argentina
Fil: Vrech, David Eduardo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto de Diversidad y Ecología Animal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto de Diversidad y Ecología Animal; Argentina
Fil: Joyce, Isabella. Desales University; Estados Unidos
Fil: Barnett, Austen A.. Desales University; Estados Unidos
Fil: Patel, Nipam H.. University of Chicago; Estados Unidos. Woods Hole; Estados Unidos
Fil: Harvey, Mark S.. Western Australian Museum; Australia
Fil: Peretti, Alfredo Vicente. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto de Diversidad y Ecología Animal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto de Diversidad y Ecología Animal; Argentina
Fil: Gulia Nuss, Monika. University Of Nevada; Estados Unidos
Fil: Sharma, Prashant P. University of Wisconsin; Estados Unidos - Materia
-
Evolutionary Biology
Functional Morphology
Developmental biology
Genes - Nivel de accesibilidad
- acceso abierto
- Condiciones de uso
- https://creativecommons.org/licenses/by/2.5/ar/
- Repositorio
- Institución
- Consejo Nacional de Investigaciones Científicas y Técnicas
- OAI Identificador
- oai:ri.conicet.gov.ar:11336/266844
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A Novel Expression Domain of extradenticle Underlies the Evolutionary Developmental Origin of the Chelicerate PatellaKlementz, Benjamin CBrenneis, GeorgHinne, Isaac A.Laumer, Ethan M.Neu, Sophie M.Hareid, Grace M.Gainett, GuilhermeSetton, Emily V. W.Simian, CatalinaVrech, David EduardoJoyce, IsabellaBarnett, Austen A.Patel, Nipam H.Harvey, Mark S.Peretti, Alfredo VicenteGulia Nuss, MonikaSharma, Prashant PEvolutionary BiologyFunctional MorphologyDevelopmental biologyGeneshttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Neofunctionalization of duplicated gene copies is thought to be an important process underlying the origin of evolutionary novelty and provides an elegant mechanism for the origin of new phenotypic traits. One putative case where a new gene copy has been linked to a novel morphological trait is the origin of the arachnid patella, a taxonomically restricted leg segment. In spiders, the origin of this segment has been linked to the origin of the paralog dachshund-2, suggesting that a new gene facilitated the expression of a new trait. However, various arachnid groups that possess patellae do not have a copy of dachshund-2, disfavoring the direct link between gene origin and trait origin. We investigated the developmental genetic basis for patellar patterning in the harvestman Phalangium opilio, which lacks dachshund-2. Here, we show that the harvestman patella is established by a novel expression domain of the transcription factor extradenticle. Leveraging this definition of patellar identity, we surveyed targeted groups across chelicerate phylogeny to assess when this trait evolved. We show that a patellar homolog is present in Pycnogonida (sea spiders) and various arachnid orders, suggesting a single origin of the patella in the ancestor of Chelicerata. A potential loss of the patella is observed in Ixodida. Our results suggest that the modification of an ancient gene, rather than the neofunctionalization of a new gene copy, underlies the origin of the patella. Broadly, this work underscores the value of comparative data and broad taxonomic sampling when testing hypotheses in evolutionary developmental biology.Fil: Klementz, Benjamin C. University of Wisconsin; Estados UnidosFil: Brenneis, Georg. Universidad de Viena; AustriaFil: Hinne, Isaac A.. University Of Nevada; Estados UnidosFil: Laumer, Ethan M.. University of Wisconsin; Estados UnidosFil: Neu, Sophie M.. University of Wisconsin; Estados UnidosFil: Hareid, Grace M.. University of Wisconsin; Estados UnidosFil: Gainett, Guilherme. Harvard Medical School; Estados Unidos. University of Wisconsin; Estados Unidos. Boston Children,’s Hospital; Estados UnidosFil: Setton, Emily V. W.. Cornell University. Department Of Ecology And Evolutionary Biology; . University of Wisconsin; Estados UnidosFil: Simian, Catalina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto de Diversidad y Ecología Animal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto de Diversidad y Ecología Animal; ArgentinaFil: Vrech, David Eduardo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto de Diversidad y Ecología Animal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto de Diversidad y Ecología Animal; ArgentinaFil: Joyce, Isabella. Desales University; Estados UnidosFil: Barnett, Austen A.. Desales University; Estados UnidosFil: Patel, Nipam H.. University of Chicago; Estados Unidos. Woods Hole; Estados UnidosFil: Harvey, Mark S.. Western Australian Museum; AustraliaFil: Peretti, Alfredo Vicente. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto de Diversidad y Ecología Animal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto de Diversidad y Ecología Animal; ArgentinaFil: Gulia Nuss, Monika. University Of Nevada; Estados UnidosFil: Sharma, Prashant P. University of Wisconsin; Estados UnidosOxford University Press2024-09info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/266844Klementz, Benjamin C; Brenneis, Georg; Hinne, Isaac A.; Laumer, Ethan M.; Neu, Sophie M.; et al.; A Novel Expression Domain of extradenticle Underlies the Evolutionary Developmental Origin of the Chelicerate Patella; Oxford University Press; Molecular Biology and Evolution; 41; 9; 9-2024; 1-210737-4038CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/mbe/article/41/9/msae188/7749772info:eu-repo/semantics/altIdentifier/doi/10.1093/molbev/msae188info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T09:54:09Zoai:ri.conicet.gov.ar:11336/266844instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-03 09:54:09.496CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse |
dc.title.none.fl_str_mv |
A Novel Expression Domain of extradenticle Underlies the Evolutionary Developmental Origin of the Chelicerate Patella |
title |
A Novel Expression Domain of extradenticle Underlies the Evolutionary Developmental Origin of the Chelicerate Patella |
spellingShingle |
A Novel Expression Domain of extradenticle Underlies the Evolutionary Developmental Origin of the Chelicerate Patella Klementz, Benjamin C Evolutionary Biology Functional Morphology Developmental biology Genes |
title_short |
A Novel Expression Domain of extradenticle Underlies the Evolutionary Developmental Origin of the Chelicerate Patella |
title_full |
A Novel Expression Domain of extradenticle Underlies the Evolutionary Developmental Origin of the Chelicerate Patella |
title_fullStr |
A Novel Expression Domain of extradenticle Underlies the Evolutionary Developmental Origin of the Chelicerate Patella |
title_full_unstemmed |
A Novel Expression Domain of extradenticle Underlies the Evolutionary Developmental Origin of the Chelicerate Patella |
title_sort |
A Novel Expression Domain of extradenticle Underlies the Evolutionary Developmental Origin of the Chelicerate Patella |
dc.creator.none.fl_str_mv |
Klementz, Benjamin C Brenneis, Georg Hinne, Isaac A. Laumer, Ethan M. Neu, Sophie M. Hareid, Grace M. Gainett, Guilherme Setton, Emily V. W. Simian, Catalina Vrech, David Eduardo Joyce, Isabella Barnett, Austen A. Patel, Nipam H. Harvey, Mark S. Peretti, Alfredo Vicente Gulia Nuss, Monika Sharma, Prashant P |
author |
Klementz, Benjamin C |
author_facet |
Klementz, Benjamin C Brenneis, Georg Hinne, Isaac A. Laumer, Ethan M. Neu, Sophie M. Hareid, Grace M. Gainett, Guilherme Setton, Emily V. W. Simian, Catalina Vrech, David Eduardo Joyce, Isabella Barnett, Austen A. Patel, Nipam H. Harvey, Mark S. Peretti, Alfredo Vicente Gulia Nuss, Monika Sharma, Prashant P |
author_role |
author |
author2 |
Brenneis, Georg Hinne, Isaac A. Laumer, Ethan M. Neu, Sophie M. Hareid, Grace M. Gainett, Guilherme Setton, Emily V. W. Simian, Catalina Vrech, David Eduardo Joyce, Isabella Barnett, Austen A. Patel, Nipam H. Harvey, Mark S. Peretti, Alfredo Vicente Gulia Nuss, Monika Sharma, Prashant P |
author2_role |
author author author author author author author author author author author author author author author author |
dc.subject.none.fl_str_mv |
Evolutionary Biology Functional Morphology Developmental biology Genes |
topic |
Evolutionary Biology Functional Morphology Developmental biology Genes |
purl_subject.fl_str_mv |
https://purl.org/becyt/ford/1.6 https://purl.org/becyt/ford/1 |
dc.description.none.fl_txt_mv |
Neofunctionalization of duplicated gene copies is thought to be an important process underlying the origin of evolutionary novelty and provides an elegant mechanism for the origin of new phenotypic traits. One putative case where a new gene copy has been linked to a novel morphological trait is the origin of the arachnid patella, a taxonomically restricted leg segment. In spiders, the origin of this segment has been linked to the origin of the paralog dachshund-2, suggesting that a new gene facilitated the expression of a new trait. However, various arachnid groups that possess patellae do not have a copy of dachshund-2, disfavoring the direct link between gene origin and trait origin. We investigated the developmental genetic basis for patellar patterning in the harvestman Phalangium opilio, which lacks dachshund-2. Here, we show that the harvestman patella is established by a novel expression domain of the transcription factor extradenticle. Leveraging this definition of patellar identity, we surveyed targeted groups across chelicerate phylogeny to assess when this trait evolved. We show that a patellar homolog is present in Pycnogonida (sea spiders) and various arachnid orders, suggesting a single origin of the patella in the ancestor of Chelicerata. A potential loss of the patella is observed in Ixodida. Our results suggest that the modification of an ancient gene, rather than the neofunctionalization of a new gene copy, underlies the origin of the patella. Broadly, this work underscores the value of comparative data and broad taxonomic sampling when testing hypotheses in evolutionary developmental biology. Fil: Klementz, Benjamin C. University of Wisconsin; Estados Unidos Fil: Brenneis, Georg. Universidad de Viena; Austria Fil: Hinne, Isaac A.. University Of Nevada; Estados Unidos Fil: Laumer, Ethan M.. University of Wisconsin; Estados Unidos Fil: Neu, Sophie M.. University of Wisconsin; Estados Unidos Fil: Hareid, Grace M.. University of Wisconsin; Estados Unidos Fil: Gainett, Guilherme. Harvard Medical School; Estados Unidos. University of Wisconsin; Estados Unidos. Boston Children,’s Hospital; Estados Unidos Fil: Setton, Emily V. W.. Cornell University. Department Of Ecology And Evolutionary Biology; . University of Wisconsin; Estados Unidos Fil: Simian, Catalina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto de Diversidad y Ecología Animal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto de Diversidad y Ecología Animal; Argentina Fil: Vrech, David Eduardo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto de Diversidad y Ecología Animal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto de Diversidad y Ecología Animal; Argentina Fil: Joyce, Isabella. Desales University; Estados Unidos Fil: Barnett, Austen A.. Desales University; Estados Unidos Fil: Patel, Nipam H.. University of Chicago; Estados Unidos. Woods Hole; Estados Unidos Fil: Harvey, Mark S.. Western Australian Museum; Australia Fil: Peretti, Alfredo Vicente. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto de Diversidad y Ecología Animal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto de Diversidad y Ecología Animal; Argentina Fil: Gulia Nuss, Monika. University Of Nevada; Estados Unidos Fil: Sharma, Prashant P. University of Wisconsin; Estados Unidos |
description |
Neofunctionalization of duplicated gene copies is thought to be an important process underlying the origin of evolutionary novelty and provides an elegant mechanism for the origin of new phenotypic traits. One putative case where a new gene copy has been linked to a novel morphological trait is the origin of the arachnid patella, a taxonomically restricted leg segment. In spiders, the origin of this segment has been linked to the origin of the paralog dachshund-2, suggesting that a new gene facilitated the expression of a new trait. However, various arachnid groups that possess patellae do not have a copy of dachshund-2, disfavoring the direct link between gene origin and trait origin. We investigated the developmental genetic basis for patellar patterning in the harvestman Phalangium opilio, which lacks dachshund-2. Here, we show that the harvestman patella is established by a novel expression domain of the transcription factor extradenticle. Leveraging this definition of patellar identity, we surveyed targeted groups across chelicerate phylogeny to assess when this trait evolved. We show that a patellar homolog is present in Pycnogonida (sea spiders) and various arachnid orders, suggesting a single origin of the patella in the ancestor of Chelicerata. A potential loss of the patella is observed in Ixodida. Our results suggest that the modification of an ancient gene, rather than the neofunctionalization of a new gene copy, underlies the origin of the patella. Broadly, this work underscores the value of comparative data and broad taxonomic sampling when testing hypotheses in evolutionary developmental biology. |
publishDate |
2024 |
dc.date.none.fl_str_mv |
2024-09 |
dc.type.none.fl_str_mv |
info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion http://purl.org/coar/resource_type/c_6501 info:ar-repo/semantics/articulo |
format |
article |
status_str |
publishedVersion |
dc.identifier.none.fl_str_mv |
http://hdl.handle.net/11336/266844 Klementz, Benjamin C; Brenneis, Georg; Hinne, Isaac A.; Laumer, Ethan M.; Neu, Sophie M.; et al.; A Novel Expression Domain of extradenticle Underlies the Evolutionary Developmental Origin of the Chelicerate Patella; Oxford University Press; Molecular Biology and Evolution; 41; 9; 9-2024; 1-21 0737-4038 CONICET Digital CONICET |
url |
http://hdl.handle.net/11336/266844 |
identifier_str_mv |
Klementz, Benjamin C; Brenneis, Georg; Hinne, Isaac A.; Laumer, Ethan M.; Neu, Sophie M.; et al.; A Novel Expression Domain of extradenticle Underlies the Evolutionary Developmental Origin of the Chelicerate Patella; Oxford University Press; Molecular Biology and Evolution; 41; 9; 9-2024; 1-21 0737-4038 CONICET Digital CONICET |
dc.language.none.fl_str_mv |
eng |
language |
eng |
dc.relation.none.fl_str_mv |
info:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/mbe/article/41/9/msae188/7749772 info:eu-repo/semantics/altIdentifier/doi/10.1093/molbev/msae188 |
dc.rights.none.fl_str_mv |
info:eu-repo/semantics/openAccess https://creativecommons.org/licenses/by/2.5/ar/ |
eu_rights_str_mv |
openAccess |
rights_invalid_str_mv |
https://creativecommons.org/licenses/by/2.5/ar/ |
dc.format.none.fl_str_mv |
application/pdf application/pdf |
dc.publisher.none.fl_str_mv |
Oxford University Press |
publisher.none.fl_str_mv |
Oxford University Press |
dc.source.none.fl_str_mv |
reponame:CONICET Digital (CONICET) instname:Consejo Nacional de Investigaciones Científicas y Técnicas |
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CONICET Digital (CONICET) |
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CONICET Digital (CONICET) |
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Consejo Nacional de Investigaciones Científicas y Técnicas |
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CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas |
repository.mail.fl_str_mv |
dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar |
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13.13397 |