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
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/266844

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network_name_str CONICET Digital (CONICET)
spelling 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
reponame_str CONICET Digital (CONICET)
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instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv 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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