Genomic Insights into Mollusk Terrestrialization: Parallel and Convergent Gene Family Expansions as Key Facilitators in Out-of-the-Sea Transitions
- Autores
- Arístide, Leandro; Fernández, Rosa
- Año de publicación
- 2023
- Idioma
- inglés
- Tipo de recurso
- artículo
- Estado
- versión publicada
- Descripción
- Animals abandoned their marine niche and successfully adapted to life on land multiple times throughout evolution, providing a rare opportunity to study the mechanisms driving large scale macroevolutionary convergence. However, the genomic factors underlying this process remain largely unknown. Here, we investigate the macroevolutionary dynamics of gene repertoire evolution during repeated transitions out of the sea in mollusks, a lineage that has transitioned to freshwater and terrestrial environments multiple independent times. Through phylogenomics and phylogenetic comparative methods, we examine ∼100 genomic data sets encompassing all major molluskan lineages. We introduce a conceptual framework for identifying and analyzing parallel and convergent evolution at the orthogroup level (groups of genes derived from a single ancestral gene in the species in question) and explore the extent of these mechanisms. Despite deep temporal divergences, we found that parallel expansions of ancient gene families played a major role in facilitating adaptation to nonmarine habitats, highlighting the relevance of the preexisting genomic toolkit in facilitating adaptation to new environments. The expanded functions primarily involve metabolic, osmoregulatory, and defense-related systems. We further found functionally convergent lineage-exclusive gene gains, while family contractions appear to be driven by neutral processes. Also, genomic innovations likely contributed to fuel independent habitat transitions. Overall, our study reveals that various mechanisms of gene repertoire evolution - parallelism, convergence, and innovation - can simultaneously contribute to major evolutionary transitions. Our results provide a genome-wide gene repertoire atlas of molluskan terrestrialization that paves the way toward further understanding the functional and evolutionary bases of this process.
Fil: Arístide, Leandro. Universitat Pompeu Fabra; España. Universidad Nacional Arturo Jauretche. Unidad Ejecutora de Estudios en Neurociencias y Sistemas Complejos. Provincia de Buenos Aires. Ministerio de Salud. Hospital Alta Complejidad en Red El Cruce Dr. Néstor Carlos Kirchner Samic. Unidad Ejecutora de Estudios en Neurociencias y Sistemas Complejos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Unidad Ejecutora de Estudios en Neurociencias y Sistemas Complejos; Argentina
Fil: Fernández, Rosa. Universitat Pompeu Fabra; España - Materia
-
COMPARATIVE GENOMICS
EVOLUTIONARY RATES
MOLLUSC
NICHE SHIFT
TERRESTRIALIZATION - Nivel de accesibilidad
- acceso abierto
- Condiciones de uso
- https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
- Repositorio
- Institución
- Consejo Nacional de Investigaciones Científicas y Técnicas
- OAI Identificador
- oai:ri.conicet.gov.ar:11336/226795
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spelling |
Genomic Insights into Mollusk Terrestrialization: Parallel and Convergent Gene Family Expansions as Key Facilitators in Out-of-the-Sea TransitionsArístide, LeandroFernández, RosaCOMPARATIVE GENOMICSEVOLUTIONARY RATESMOLLUSCNICHE SHIFTTERRESTRIALIZATIONhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Animals abandoned their marine niche and successfully adapted to life on land multiple times throughout evolution, providing a rare opportunity to study the mechanisms driving large scale macroevolutionary convergence. However, the genomic factors underlying this process remain largely unknown. Here, we investigate the macroevolutionary dynamics of gene repertoire evolution during repeated transitions out of the sea in mollusks, a lineage that has transitioned to freshwater and terrestrial environments multiple independent times. Through phylogenomics and phylogenetic comparative methods, we examine ∼100 genomic data sets encompassing all major molluskan lineages. We introduce a conceptual framework for identifying and analyzing parallel and convergent evolution at the orthogroup level (groups of genes derived from a single ancestral gene in the species in question) and explore the extent of these mechanisms. Despite deep temporal divergences, we found that parallel expansions of ancient gene families played a major role in facilitating adaptation to nonmarine habitats, highlighting the relevance of the preexisting genomic toolkit in facilitating adaptation to new environments. The expanded functions primarily involve metabolic, osmoregulatory, and defense-related systems. We further found functionally convergent lineage-exclusive gene gains, while family contractions appear to be driven by neutral processes. Also, genomic innovations likely contributed to fuel independent habitat transitions. Overall, our study reveals that various mechanisms of gene repertoire evolution - parallelism, convergence, and innovation - can simultaneously contribute to major evolutionary transitions. Our results provide a genome-wide gene repertoire atlas of molluskan terrestrialization that paves the way toward further understanding the functional and evolutionary bases of this process.Fil: Arístide, Leandro. Universitat Pompeu Fabra; España. Universidad Nacional Arturo Jauretche. Unidad Ejecutora de Estudios en Neurociencias y Sistemas Complejos. Provincia de Buenos Aires. Ministerio de Salud. Hospital Alta Complejidad en Red El Cruce Dr. Néstor Carlos Kirchner Samic. Unidad Ejecutora de Estudios en Neurociencias y Sistemas Complejos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Unidad Ejecutora de Estudios en Neurociencias y Sistemas Complejos; ArgentinaFil: Fernández, Rosa. Universitat Pompeu Fabra; EspañaOxford University Press2023-10info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/226795Arístide, Leandro; Fernández, Rosa; Genomic Insights into Mollusk Terrestrialization: Parallel and Convergent Gene Family Expansions as Key Facilitators in Out-of-the-Sea Transitions; Oxford University Press; Genome Biology and Evolution; 15; 10; 10-2023; 1-171759-6653CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1093/gbe/evad176info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:32:15Zoai:ri.conicet.gov.ar:11336/226795instacron: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:34982025-09-29 10:32:15.619CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse |
dc.title.none.fl_str_mv |
Genomic Insights into Mollusk Terrestrialization: Parallel and Convergent Gene Family Expansions as Key Facilitators in Out-of-the-Sea Transitions |
title |
Genomic Insights into Mollusk Terrestrialization: Parallel and Convergent Gene Family Expansions as Key Facilitators in Out-of-the-Sea Transitions |
spellingShingle |
Genomic Insights into Mollusk Terrestrialization: Parallel and Convergent Gene Family Expansions as Key Facilitators in Out-of-the-Sea Transitions Arístide, Leandro COMPARATIVE GENOMICS EVOLUTIONARY RATES MOLLUSC NICHE SHIFT TERRESTRIALIZATION |
title_short |
Genomic Insights into Mollusk Terrestrialization: Parallel and Convergent Gene Family Expansions as Key Facilitators in Out-of-the-Sea Transitions |
title_full |
Genomic Insights into Mollusk Terrestrialization: Parallel and Convergent Gene Family Expansions as Key Facilitators in Out-of-the-Sea Transitions |
title_fullStr |
Genomic Insights into Mollusk Terrestrialization: Parallel and Convergent Gene Family Expansions as Key Facilitators in Out-of-the-Sea Transitions |
title_full_unstemmed |
Genomic Insights into Mollusk Terrestrialization: Parallel and Convergent Gene Family Expansions as Key Facilitators in Out-of-the-Sea Transitions |
title_sort |
Genomic Insights into Mollusk Terrestrialization: Parallel and Convergent Gene Family Expansions as Key Facilitators in Out-of-the-Sea Transitions |
dc.creator.none.fl_str_mv |
Arístide, Leandro Fernández, Rosa |
author |
Arístide, Leandro |
author_facet |
Arístide, Leandro Fernández, Rosa |
author_role |
author |
author2 |
Fernández, Rosa |
author2_role |
author |
dc.subject.none.fl_str_mv |
COMPARATIVE GENOMICS EVOLUTIONARY RATES MOLLUSC NICHE SHIFT TERRESTRIALIZATION |
topic |
COMPARATIVE GENOMICS EVOLUTIONARY RATES MOLLUSC NICHE SHIFT TERRESTRIALIZATION |
purl_subject.fl_str_mv |
https://purl.org/becyt/ford/1.6 https://purl.org/becyt/ford/1 |
dc.description.none.fl_txt_mv |
Animals abandoned their marine niche and successfully adapted to life on land multiple times throughout evolution, providing a rare opportunity to study the mechanisms driving large scale macroevolutionary convergence. However, the genomic factors underlying this process remain largely unknown. Here, we investigate the macroevolutionary dynamics of gene repertoire evolution during repeated transitions out of the sea in mollusks, a lineage that has transitioned to freshwater and terrestrial environments multiple independent times. Through phylogenomics and phylogenetic comparative methods, we examine ∼100 genomic data sets encompassing all major molluskan lineages. We introduce a conceptual framework for identifying and analyzing parallel and convergent evolution at the orthogroup level (groups of genes derived from a single ancestral gene in the species in question) and explore the extent of these mechanisms. Despite deep temporal divergences, we found that parallel expansions of ancient gene families played a major role in facilitating adaptation to nonmarine habitats, highlighting the relevance of the preexisting genomic toolkit in facilitating adaptation to new environments. The expanded functions primarily involve metabolic, osmoregulatory, and defense-related systems. We further found functionally convergent lineage-exclusive gene gains, while family contractions appear to be driven by neutral processes. Also, genomic innovations likely contributed to fuel independent habitat transitions. Overall, our study reveals that various mechanisms of gene repertoire evolution - parallelism, convergence, and innovation - can simultaneously contribute to major evolutionary transitions. Our results provide a genome-wide gene repertoire atlas of molluskan terrestrialization that paves the way toward further understanding the functional and evolutionary bases of this process. Fil: Arístide, Leandro. Universitat Pompeu Fabra; España. Universidad Nacional Arturo Jauretche. Unidad Ejecutora de Estudios en Neurociencias y Sistemas Complejos. Provincia de Buenos Aires. Ministerio de Salud. Hospital Alta Complejidad en Red El Cruce Dr. Néstor Carlos Kirchner Samic. Unidad Ejecutora de Estudios en Neurociencias y Sistemas Complejos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Unidad Ejecutora de Estudios en Neurociencias y Sistemas Complejos; Argentina Fil: Fernández, Rosa. Universitat Pompeu Fabra; España |
description |
Animals abandoned their marine niche and successfully adapted to life on land multiple times throughout evolution, providing a rare opportunity to study the mechanisms driving large scale macroevolutionary convergence. However, the genomic factors underlying this process remain largely unknown. Here, we investigate the macroevolutionary dynamics of gene repertoire evolution during repeated transitions out of the sea in mollusks, a lineage that has transitioned to freshwater and terrestrial environments multiple independent times. Through phylogenomics and phylogenetic comparative methods, we examine ∼100 genomic data sets encompassing all major molluskan lineages. We introduce a conceptual framework for identifying and analyzing parallel and convergent evolution at the orthogroup level (groups of genes derived from a single ancestral gene in the species in question) and explore the extent of these mechanisms. Despite deep temporal divergences, we found that parallel expansions of ancient gene families played a major role in facilitating adaptation to nonmarine habitats, highlighting the relevance of the preexisting genomic toolkit in facilitating adaptation to new environments. The expanded functions primarily involve metabolic, osmoregulatory, and defense-related systems. We further found functionally convergent lineage-exclusive gene gains, while family contractions appear to be driven by neutral processes. Also, genomic innovations likely contributed to fuel independent habitat transitions. Overall, our study reveals that various mechanisms of gene repertoire evolution - parallelism, convergence, and innovation - can simultaneously contribute to major evolutionary transitions. Our results provide a genome-wide gene repertoire atlas of molluskan terrestrialization that paves the way toward further understanding the functional and evolutionary bases of this process. |
publishDate |
2023 |
dc.date.none.fl_str_mv |
2023-10 |
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/11336/226795 Arístide, Leandro; Fernández, Rosa; Genomic Insights into Mollusk Terrestrialization: Parallel and Convergent Gene Family Expansions as Key Facilitators in Out-of-the-Sea Transitions; Oxford University Press; Genome Biology and Evolution; 15; 10; 10-2023; 1-17 1759-6653 CONICET Digital CONICET |
url |
http://hdl.handle.net/11336/226795 |
identifier_str_mv |
Arístide, Leandro; Fernández, Rosa; Genomic Insights into Mollusk Terrestrialization: Parallel and Convergent Gene Family Expansions as Key Facilitators in Out-of-the-Sea Transitions; Oxford University Press; Genome Biology and Evolution; 15; 10; 10-2023; 1-17 1759-6653 CONICET Digital CONICET |
dc.language.none.fl_str_mv |
eng |
language |
eng |
dc.relation.none.fl_str_mv |
info:eu-repo/semantics/altIdentifier/doi/10.1093/gbe/evad176 |
dc.rights.none.fl_str_mv |
info:eu-repo/semantics/openAccess https://creativecommons.org/licenses/by-nc-sa/2.5/ar/ |
eu_rights_str_mv |
openAccess |
rights_invalid_str_mv |
https://creativecommons.org/licenses/by-nc-sa/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) |
collection |
CONICET Digital (CONICET) |
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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1844614335485181952 |
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13.070432 |