Cargando…

Convergent deployment of ancestral functions during the evolution of mammalian flight membranes

Lateral flight membranes, or patagia, have evolved repeatedly in diverse mammalian lineages. While little is known about patagium development, its recurrent evolution may suggest a shared molecular basis. By combining transcriptomics, developmental experiments, and mouse transgenics, we demonstrate...

Descripción completa

Detalles Bibliográficos
Autores principales: Feigin, Charles Y., Moreno, Jorge A., Ramos, Raul, Mereby, Sarah A., Alivisatos, Ares, Wang, Wei, van Amerongen, Renée, Camacho, Jasmin, Rasweiler, John J., Behringer, Richard R., Ostrow, Bruce, Plikus, Maksim V., Mallarino, Ricardo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Association for the Advancement of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10038344/
https://www.ncbi.nlm.nih.gov/pubmed/36961889
http://dx.doi.org/10.1126/sciadv.ade7511
_version_ 1784912059407794176
author Feigin, Charles Y.
Moreno, Jorge A.
Ramos, Raul
Mereby, Sarah A.
Alivisatos, Ares
Wang, Wei
van Amerongen, Renée
Camacho, Jasmin
Rasweiler, John J.
Behringer, Richard R.
Ostrow, Bruce
Plikus, Maksim V.
Mallarino, Ricardo
author_facet Feigin, Charles Y.
Moreno, Jorge A.
Ramos, Raul
Mereby, Sarah A.
Alivisatos, Ares
Wang, Wei
van Amerongen, Renée
Camacho, Jasmin
Rasweiler, John J.
Behringer, Richard R.
Ostrow, Bruce
Plikus, Maksim V.
Mallarino, Ricardo
author_sort Feigin, Charles Y.
collection PubMed
description Lateral flight membranes, or patagia, have evolved repeatedly in diverse mammalian lineages. While little is known about patagium development, its recurrent evolution may suggest a shared molecular basis. By combining transcriptomics, developmental experiments, and mouse transgenics, we demonstrate that lateral Wnt5a expression in the marsupial sugar glider (Petaurus breviceps) promotes the differentiation of its patagium primordium. We further show that this function of Wnt5a reprises ancestral roles in skin morphogenesis predating mammalian flight and has been convergently used during patagium evolution in eutherian bats. Moreover, we find that many genes involved in limb development have been redeployed during patagium outgrowth in both the sugar glider and bat. Together, our findings reveal that deeply conserved genetic toolkits contribute to the evolutionary transition to flight in mammals.
format Online
Article
Text
id pubmed-10038344
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher American Association for the Advancement of Science
record_format MEDLINE/PubMed
spelling pubmed-100383442023-03-25 Convergent deployment of ancestral functions during the evolution of mammalian flight membranes Feigin, Charles Y. Moreno, Jorge A. Ramos, Raul Mereby, Sarah A. Alivisatos, Ares Wang, Wei van Amerongen, Renée Camacho, Jasmin Rasweiler, John J. Behringer, Richard R. Ostrow, Bruce Plikus, Maksim V. Mallarino, Ricardo Sci Adv Earth, Environmental, Ecological, and Space Sciences Lateral flight membranes, or patagia, have evolved repeatedly in diverse mammalian lineages. While little is known about patagium development, its recurrent evolution may suggest a shared molecular basis. By combining transcriptomics, developmental experiments, and mouse transgenics, we demonstrate that lateral Wnt5a expression in the marsupial sugar glider (Petaurus breviceps) promotes the differentiation of its patagium primordium. We further show that this function of Wnt5a reprises ancestral roles in skin morphogenesis predating mammalian flight and has been convergently used during patagium evolution in eutherian bats. Moreover, we find that many genes involved in limb development have been redeployed during patagium outgrowth in both the sugar glider and bat. Together, our findings reveal that deeply conserved genetic toolkits contribute to the evolutionary transition to flight in mammals. American Association for the Advancement of Science 2023-03-24 /pmc/articles/PMC10038344/ /pubmed/36961889 http://dx.doi.org/10.1126/sciadv.ade7511 Text en Copyright © 2023 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). https://creativecommons.org/licenses/by-nc/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license (https://creativecommons.org/licenses/by-nc/4.0/) , which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.
spellingShingle Earth, Environmental, Ecological, and Space Sciences
Feigin, Charles Y.
Moreno, Jorge A.
Ramos, Raul
Mereby, Sarah A.
Alivisatos, Ares
Wang, Wei
van Amerongen, Renée
Camacho, Jasmin
Rasweiler, John J.
Behringer, Richard R.
Ostrow, Bruce
Plikus, Maksim V.
Mallarino, Ricardo
Convergent deployment of ancestral functions during the evolution of mammalian flight membranes
title Convergent deployment of ancestral functions during the evolution of mammalian flight membranes
title_full Convergent deployment of ancestral functions during the evolution of mammalian flight membranes
title_fullStr Convergent deployment of ancestral functions during the evolution of mammalian flight membranes
title_full_unstemmed Convergent deployment of ancestral functions during the evolution of mammalian flight membranes
title_short Convergent deployment of ancestral functions during the evolution of mammalian flight membranes
title_sort convergent deployment of ancestral functions during the evolution of mammalian flight membranes
topic Earth, Environmental, Ecological, and Space Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10038344/
https://www.ncbi.nlm.nih.gov/pubmed/36961889
http://dx.doi.org/10.1126/sciadv.ade7511
work_keys_str_mv AT feigincharlesy convergentdeploymentofancestralfunctionsduringtheevolutionofmammalianflightmembranes
AT morenojorgea convergentdeploymentofancestralfunctionsduringtheevolutionofmammalianflightmembranes
AT ramosraul convergentdeploymentofancestralfunctionsduringtheevolutionofmammalianflightmembranes
AT merebysaraha convergentdeploymentofancestralfunctionsduringtheevolutionofmammalianflightmembranes
AT alivisatosares convergentdeploymentofancestralfunctionsduringtheevolutionofmammalianflightmembranes
AT wangwei convergentdeploymentofancestralfunctionsduringtheevolutionofmammalianflightmembranes
AT vanamerongenrenee convergentdeploymentofancestralfunctionsduringtheevolutionofmammalianflightmembranes
AT camachojasmin convergentdeploymentofancestralfunctionsduringtheevolutionofmammalianflightmembranes
AT rasweilerjohnj convergentdeploymentofancestralfunctionsduringtheevolutionofmammalianflightmembranes
AT behringerrichardr convergentdeploymentofancestralfunctionsduringtheevolutionofmammalianflightmembranes
AT ostrowbruce convergentdeploymentofancestralfunctionsduringtheevolutionofmammalianflightmembranes
AT plikusmaksimv convergentdeploymentofancestralfunctionsduringtheevolutionofmammalianflightmembranes
AT mallarinoricardo convergentdeploymentofancestralfunctionsduringtheevolutionofmammalianflightmembranes