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
CONICET Digital (CONICET)
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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